Journal of Human Evolution 174 (2023) 103296

Contents lists available at ScienceDirect

Journal of Human Evolution

journal homepage: www.elsevier.com/locate/jhevol

Moving beyond the adaptationist paradigm for human evolution, and

why it matters
Lauren Schroeder a, b, *, Rebecca Rogers Ackermann b, c, *
a
Department of Anthropology, University of Toronto Mississauga, Mississauga, ON, L5L 1C6, Canada
b
Human Evolution Research Institute, University of Cape Town, Rondebosch, 7701, South Africa
c
Department of Archaeology, University of Cape Town, Rondebosch, 7701, South Africa

a r t i c l e i n f o a b s t r a c t

Article history: The Journal of Human Evolution (JHE) was founded 50 years ago when much of the foundation for how
Received 25 April 2022 we think about human evolution was in place or being put in place, providing the main framework for
Accepted 12 November 2022 how we consider our origins today. Here, we will explore historical developments, including early JHE
Available online 15 December 2022
outputs, as they relate to our understanding of the relationship between phenotypic variation and
evolutionary process, and use that as a springboard for considering our current understanding of these
Keywords:
links as applied to human evolution. We will focus specifically on how the study of variation itself has
Genetic drift
shifted us away from taxonomic and adaptationist perspectives toward a richer understanding of the
Hybridization
Neutral evolution
processes shaping human evolutionary history, using literature searches and specific test cases to
Natural selection highlight this. We argue that natural selection, gene exchange, genetic drift, and mutation should not be
Phenotypic variation considered individually when considering the production of hominin diversity. In this context, we offer
Evolutionary process suggestions for future research directions and reflect on this more complex understanding of human
evolution and its broader relevance to society. Finally, we end by considering authorship demographics
and practices in the last 50 years within JHE and how a shift in these demographics has the potential to
reshape the science of human evolution going forward.
© 2022 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND
license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction this classificatory framework, consideration of variation is

1.1. Why study variation?
In the same way that early researchers sought to find key dif-
ferences that separated groups of living people into ‘races,’
paleoanthropologists have historically (and even today) taken a
similar typological approach when assessing fossil morphology
(Wolpoff and Caspari, 2000; Marks, 2007; Athreya and Hopkins,
2021). By its very nature, the diagnosis of ‘difference’ necessary
for making taxonomic assessments, as defined by the Interna-
tional Commission on Zoological Nomenclature (ICZN), compares
new specimens to existing hypodigms constructed around a single
holotype individual (ICZN, 1999). Where fossil finds are rare, such
as in paleoanthropology, type specimens are often used to
represent the average of a species by historical accident rather
than because all variation in the species is actually known. Within
* Corresponding authors.
E-mail addresses: lauren.schroeder@utoronto.ca (L. Schroeder),
ackermann@uct.ac.za (R.R. Ackermann).
predominantly used as a means for determining how different
two fossils have to be put into different species or subspecies,
information marshaled for the reconstruction of phylogenetic
relationships, rather than being a direct focus of study. In addition
to approaching variation through a decidedly typological frame-
work, these approaches also frequently (and largely uncon-
sciously) narrate our origins through a colonial and racialized lens,
a historical legacy of otherizing some and elevating others
(Wolpoff and Caspari, 2000; Athreya and Ackermann, 2020;
Athreya and Hopkins, 2021).
But understanding phenotypic variation goes well beyond
taxonomic utility, as it provides a link between pattern and process,
allowing us to concentrate on the dynamics of human evolution.
We know that most traits of interest to paleoanthropology have a
complex genetic basis (Lewontin, 1974; Lynch and Walsh, 1998;
Houle et al., 2010; Boyle et al., 2017), being continuous, and
therefore generally polygenic, i.e., influenced by more than one
gene. In general, we have a limited grasp of the genetic un-
derpinnings of such morphology (e.g., Mathieson, 2021), with a few
becky. exceptions (e.g., Aponte, et al., 2021), and while paleogenetic
studies can and do provide some insight into evolutionary process,

https://doi.org/10.1016/j.jhevol.2022.103296
0047-2484/© 2022 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
L. Schroeder and R.R. Ackermann
they often necessarily concentrate on genes of large effect (e.g.,
Lalueza-Fox et al., 2007; Mathieson et al., 2015; Irving-Pease et al.,
2021). Importantly, a focus on morphological variation provides a
complementary perspective for understanding these processes.
However, this focus on phenotypic variation has often resulted in a
tendency toward adaptationist thinking, resulting in the prevalence
of what we term the ‘adaptationist paradigm’ in human evolution,
i.e., a conceptual framework underlying paleoanthropological
research that a specific function or adaptation underlies most or
even all of the variation that we see in the human fossil record.
Here we will briefly reflect on the state of the science when the
Journal of Human Evolution (JHE) was first established, in terms of
our general understanding of hominin diversity, evolutionary
process, and phylogenetic relationships. We will then take a his-
torical perspective, including honing in on early JHE papers that can
be seen as early approaches for considering the link between
variation and evolutionary process, specifically focusing on gene
exchange and genetic drift, using these as a springboard for
exploring where we are today, and where we might go in the
future. We will specifically look at how a variation-based approach
to understanding evolution has moved us well beyond simplistic
adaptationist narratives of the past by demonstrating how different
evolutionary forces work in concert to shape hominin diversity.
This, in turn, has societal implications for how we interpret
diversity. We conclude by reflecting on a different kind of variation,
i.e., demographics of authorship, and how this has the potential to
reshape the science of human evolution going forward.
1.2. A snapshot of hominin diversity 50 years ago
In the early 1970s when JHE was established, many researchers
still referred to Hominidae, including humans and their extinct
relatives, as separate from Pongidae (the large-bodied apes), as this
predated the phylogenetic revision based on our molecular
understanding of the close relationship between humans and
chimpanzees. Indeed, there was limited molecular understanding
of detailed relationships at all, but this was slowly changing with
advances being made in molecular genetics (e.g., Hoyer et al., 1972).
At this time, known hominin diversity consisted of only a select
number of taxa from the Homo lineage (Homo habilis, Homo erectus,
Neanderthals, Homo sapiens), and a handful of taxa that were
historically lumped into the single genus Australopithecus (i.e.,
Australopithecus africanus, Australopithecus robustus, and Austral-
opithecus boisei as shown in Fig. 1A sensu Delson et al., 1977). Well-
associated archaeology was also fairly limited (Isaac, 1975). The
bushy family tree that is so often depicted today was not relevant to
this sparse diversity of hominins, and generally, taxonomic argu-
ments centered on whether the genus Homo was separate from and
contemporaneous with Australopithecus (e.g., Robinson, 1954;
Leakey and Wood, 1973; Robinson and Steudel, 1973), or not (e.g.,
Wolpoff, 1971). Owing to this paucity of fossil taxa, the genus Homo
was largely considered to be anagenetic from H. erectus
onwarddthough much of this discussion was shaped slightly later,
during the 1980s multiregional evolution (MRE) vs. recent African
origin argument related to the emergence of H. sapiens (Thorne and
Wolpoff, 1981; Bra €uer, 1984; Wolpoff et al., 1984; Stringer and
Andrews, 1988). The stark difference between what was known
about hominin diversity then vs. typical depictions today is illus-
trated in Figure 1.
As we will discuss further below, adaptation via natural selec-
tion was the primary explanation for the production of hominin
diversity. There was little attention paid to genetic drift and
nonadaptive processes, given that the journal was established in
1972, only a few years after Kimura (1968) proposed the neutral
theory of evolution, and before both Gould and Lewontin's (1979)
2
Journal of Human Evolution 174 (2023) 103296
classic paper critiquing the ‘adaptationist programme’ and
Lande's (1976) incorporation of aspects of the neutral theory into a
quantitative genetic framework allowing for the evaluation of fos-
sils directly. The discussion of hybridization and its effects was also
limited, and was centered primarily within the ‘modern human
origins’ context, i.e., whether in an MRE model gene exchange
existed between the potentially divergent lineages that lead
(collectively) to ‘modern’ people (e.g., Wolpoff et al., 1984).
Since these early days of JHE, our understanding of the
complexities of human evolution, including our understanding of
phenotypic variation, has changed dramatically. We now have a
fossil record that is both deeper in time and considerably more
speciose (Fig. 1B), even by conservative estimates. Early hominins
are present as early as 6e7 Ma, and there are many points in time
where species are contemporaneous. Advances in genetics have
allowed for the analysis of both living taxa and paleotaxa, providing
previously unavailable insight into phylogenetic relationships,
hybridization, and an overall deeper understanding of the rela-
tionship between genotype and phenotype (reviews in Gokcumen,
2020; Irving-Pease et al., 2021). In addition, developments in
evolutionary quantitative genetics have expanded our investiga-
tory power of evolutionary processes in the fossil record (e.g.,
Hlusko et al., 2016; Melo et al., 2016; Weaver and Gunz, 2018; Brasil
et al., 2020; reviews in Weaver, 2018; von Cramon-Taubadel, 2019).
Within this context, the approach to considering the production of
variation has broadened from one that was primarily adaptationist
to one that increasingly incorporates genetic drift and gene
exchange as important forces shaping the trajectory of human
evolution. We will highlight these advances in the next few sections
of this paper, and provide examples of early papers in the journal
that were pioneering in this regard.
2. Quantitative genetics and genetic drift in human
evolutionary studies
2.1. Historical developments
The fundamental mathematical underpinnings of theoretical
population genetics were formulated in the early 20th century
through the work of S. Wright, R.A. Fisher, and J.B.S. Haldane
(Provine, 1971). Fisher's (1918) groundbreaking paper formed the
basis for this development, specifically the recognition that
phenotypic traits are polygenic, and that their inheritance does not
follow a simple Mendelian model. While this advancement in the
field of genetics provided a more sophisticated, more quantitative
approach to evolutionary modeling, the primary process of evolu-
tion (i.e., genetic drift, natural selection, mutation) was a matter of
contention. A good illustration of this is the contrasting viewpoints
of two of population genetics' co-founders. Wright hypothesized
that genetic drift, acting in small populations, may be an important
force driving evolutionary change (Wright, 1931, 1932, 1970), while
Fisher viewed genetic drift as insignificant, and saw adaptive
evolution through natural selection as the sole and most significant
process (Fisher, 1930). This latter view, termed ‘panselectionism’ by
M. Kimura (1983) and discussed in great detail in Gould and Lew-
ontin's critique of the ‘adaptationist program’ (Gould and Lewontin,
1979), was much more broadly accepted by biologists, becoming an
almost ubiquitously held position in both genetics and morpho-
logical studies in the mid-20th century.
One significant deviation from this view came in 1953 when
G.G. Simpson considered the possible effect that genetic drift may
have had on morphological evolution in the fossil record (Simpson,
1953). Simpson introduced the theoretical model of adaptive zones
for driving rapid evolution, hypothesizing that these zones were
dominated by stabilizing selection, but that genetic drift may have
L. Schroeder and R.R. Ackermann
Figure 1. Comparing a commonly held view of human evolution in 1977 (A) with our contemporary understanding of hominin diversity (B). Temporal ranges of known fossil
hominins are taken from Wood and McRae (2021). Panel A is reprinted from Delson et al. (1977), with permission from Elsevier. Silhouettes in panel B are taken from PhyloPic
(http://phylopic.org).
played an important role when these adaptive zones were crossed
(Simpson, 1953). Loosely mirroring Wright's ‘shifting balance
theory’ for genotypes (Wright, 1932), this hypothesis represented a
direct application of population genetics theory to the fossil record.
This expansion into macroevolutionary considerations reflected the
growing acceptance and applicability of the synthetic theory or
‘Modern synthesis’ of evolution (Huxley, 1942). However, what was
lacking at the time was a bridge between population genetics with
its mathematical formulae and allele frequencies that could only be
indirectly and inferentially applied to phenotypes, and actual
evolutionary change at a genotypic level (Kimura, 1983; von
Cramon-Taubadel, 2019).
This all changed in the mid-1960s with the development of
molecular genetics. Researchers succeeded in determining the
amino acid sequences of several proteins found among vertebrate
taxa, a breakthrough that provided the first opportunity for
comparing the amount and rate of molecular change among species
(Zuckerkandl and Pauling, 1965a). In addition, the detection of
genetic polymorphisms within species allowed for a more detailed
estimation of intrapopulation variability (Lewontin and Hubby,
1966). With these two developments, researchers were finally
able to apply mathematical models of population genetics to
empirical data, and it was against this backdrop that the neutral
theory of evolution was proposed.
2.2. The neutral theory
The neutral theory of molecular evolution, or the neutral
mutation-random drift hypothesis, claims that most evolutionary
changes are due to random genetic drift (random fixation) of
selectively neutral or nearly neutral mutants, which are those that
are equivalent in terms of fitness (Kimura, 1968, 1983, 1991). The
theory rests mainly on the following premises. First, the rate of
amino acid or nucleotides substitutions is constant across many
3
Journal of Human Evolution 174 (2023) 103296
lineages (a concept known as the ‘molecular clock’). Second, these
substitutions occur at a much higher rate than would be expected if
most substitutions were adaptive or beneficial, as previously
calculated by Haldane (1957). And third, synonymous substitutions
in noncoding regions of the DNA that do not lead to changes in
amino acids occur at a much greater rate than nonsynonymous
substitutions that do cause amino acid changes (Zuckerkandl and
Pauling, 1965b; Salser, 1978). These synonymous substitutions are
essentially invisible to natural selection, yet they represent the
majority of changes.
An important aspect of the neutral theory that should be
underlined is that it does not disregard the action of natural
selection entirely. This is a common misconception that has fueled
many of the criticisms leveled against it as the theory does
emphasize the action of purifying selection, for removing delete-
rious alleles, as playing a large role in neutral explanations (Kimura,
1983). Overall, the neutral theory provides a testable mathematical
framework for application to empirical data, specifically a useful
null hypothesis (genetic drift) that if rejected can point to the action
of other evolutionary processes (Kreitman, 1996). While this theory
shifted the dominant adaptationist narrative of evolutionary
change, and hence represented a major contribution to the field of
population genetics, application to phenotypic evolution had not
yet been operationalized.
2.3. Quantitative genetics as a means to move beyond the
adaptationist paradigm
The application of the neutral theory to morphological data was
developed through approaches rooted in evolutionary quantitative
genetics, which is the study of the evolution of continuous or
‘quantitative’ traits and their underlying genetics (Falconer, 1960;
Lande, 2000; von Cramon-Taubadel and Schroeder, 2018). Foun-
dational to this framework is the notion of pleiotropy, the effect of a
L. Schroeder and R.R. Ackermann
single gene on multiple phenotypic traits, and R. Fisher's 1918
framework of polygenic inheritance, which describes phenotypic
traits that are affected by gene variants at multiple loci. These two
concepts emphasize the importance of genetic and phenotypic
variance and covariance as basic measures in quantitative genetic
theory (Provine, 1971).
Another important concept relates to the relationship between
genotype and phenotype, and its connection to heritability. The
basic model of this relationship is that the phenotypic variance of a
quantitative trait (VP) can be partitioned into genetic variance (VG),
environmental components (VE), and the interaction between
these genetic and environmental components (VGE). As a result of
the polygenic inheritance of quantitative traits, the VG component
is composed of three sources of genetic variance: additive genetic
variance, variance attributed to dominance effects, and variance
attributed to epistatic interactions (Cheverud, 1988; Lynch and
Walsh, 1998). Of these three sources of variance, the additive
genetic variance (VA), which refers to variance attributable to the
additive effects of all inherited gene loci that contribute to a
particular quantitative trait, is central to the calculation of narrow-
sense heritability (h2), the proportion of VP that can be ascribed to
VA (Falconer and Mackay, 1996; Lynch and Walsh, 1998). This
measure can be estimated through studies of pedigreed organisms
(e.g., Carson, 2006; Hlusko et al., 2006; Roseman et al., 2010).
Narrow-sense heritability is a fundamental variable in the classic
quantitative genetics Breeder's equation (R ¼ h2s), and essentially
provides an estimate of the extent to which a quantitative trait
responds to selection, where R is the trait response, and s is the
selection differential calculated as the difference between the mean
of the trait before and after selection (Falconer, 1960). This equation
is central to much of the subsequent contributions to the field,
especially in the application of principles of the neutral theory to
phenotypic evolution.
In 1976, R. Lande developed a theory of evolution, building on
the Breeder's equation (Equation 1 in Lande, 1976), that incorpo-
rated aspects of the neutral theory within a quantitative genetic
framework to allow for the evaluation of univariate phenotypic
outcomes in fossil populations under models of random genetic
drift or natural selection, marking a turning point in evolutionary
studies. This classic paper also provided the first iteration of a test
for the null hypothesis of genetic drift based on rates of evolution
and effective population size, as well as a model for testing
Simpson's (1953) proposal of adaptive zones in macroevolution
(Lande, 1976). An additional noteworthy point in this paper that
Lande highlights are the difficulties inherent in the estimation of
heritability for fossil populations. He overcomes this by using
assumptions based on mammalian models to estimate heritability
values in the fossil groups being analyzing (Lande, 1976), something
that is commonplace today (e.g., Cheverud, 1988; Schroeder et al.,
2014; Baab, 2018; Irish and Grabowski, 2021; Machado et al., 2022).
Subsequently, many new contributions to the field of quantita-
tive genetics were made; however, these early studies were
restricted in terms of their application to multivariate quantitative
traits and trait covariance, something that Darwin (1859) also
recognized as important for fully understanding the morphological
response to selective pressures. Another landmark study by Lande
(1979) provided a solution to this issue with the formulation of
the multivariate Breeder's equation. The so-called Lande equation
(Dz ¼ Gb) presents the relationship between a vector of trait
responses in a population (the difference in those traits before and
after selection) as a function of the product of the G-matrix (the
additive genetic variance/covariance matrix underlying those traits
in the population) and the vector of selection coefficients (selection
gradient) acting on those traits (b). The G-matrix is composed of the
additive genetic variance of each trait along the diagonal (VA), and
4
Journal of Human Evolution 174 (2023) 103296
the additive genetic covariances among the traits on the off-
diagonal. The relationship between traits at a genetic level that is
captured by the G-matrix greatly affects how each trait can respond
to the selection gradient (b) in terms of both direction and strength.
If traits are highly integrated (covary), then they are constrained to
follow a similar pattern of directional response to the selection
pressure, even if selection is acting in multiple directions. In
contrast, if traits do not covary, they will follow the direction of
each separate selection coefficient.
Lande and Arnold (1983) provided an extension of this principle
as a way of determining the forces of selection acting directly on
traits. This is carried out through the equation: b ¼ P1 s, which
considers selection gradients as partial regression coefficients of
fitness on traits. In this equation, P1 is the inverse of the pheno-
typic variance/covariance matrix of the traits in question, and s is a
vector of directional selection differentials, i.e., the differences be-
tween trait means before and after selection. If morphological traits
covary significantly, there may be a mismatch in the direction of
selection and response to that selection, resulting in instances of
indirect selection acting on these selection differentials that
therefore do not confer a fitness benefit.
Another major insight from Lande (1979) is that for diverging
populations under a null hypothesis of genetic drift, the variation of
traits after time t is a function of the G-matrix and the size of these
populations. The relationship is given by B ¼ G Nte, where B is the
between-population variance/covariance matrix, t is the time since
divergence, Ne is the effective population size, and G is the additive
genetic variance/covariance matrix of the source population.
Furthermore, under genetic drift, it is expected that this between-
group variability (B) is proportional to G. If t and Ne are known,
tests of rates of evolution can be performed through the calculation


of the generalized genetic distance Nte Dz0 G1 Dz , which follows a
c2 distribution under genetic drift, with degrees of freedom equal
to the number of traits. Using a 95% confidence interval, one can
also determine if rates are lower than expected (stabilizing selec-
tion), or higher than expected (diversifying selection).
These equations and developments have formed the basis for
several important advances in the applicability of these techniques
to phenotypic data, especially after a landmark study by Cheverud
(1988) provided evidence for the proportionality of G and P
matrices (see Roff, 1995 and Sodini et al., 2018 for further support of
‘Cheverud's conjecture’), allowing for the substitution of P for G
(i.e., phenotype for genotype) in many of the equations given above.
In addition, today we know that for most quantitative morpho-
logical traits of interest, heritability estimates range between 0.3
and 0.5. So like Lande (1976), we make reasonable assumptions of
heritabilities based on data from related organisms (e.g., Roseman
et al., 2010), which we can then use to correct our P-matrix.
More recently, Ackermann and Cheverud (2002) extended the
utility of an aspect of Lande's theory, namely the expected
proportionality of G and B across groups (a minimum of two at any
taxonomic level) under genetic drift, by developing a test of this
null hypothesis based on linear regression and principal compo-
nent analysis (PCA). First, given the proportionality of G and P (as
per Cheverud, 1988), P is substituted for G. Second, P is decomposed
into its principal components, and B is calculated by finding the
variance among principal components projected onto the group
means. Third, the log-transformed among-group variances (esti-
mated B) are regressed on the log-transformed eigenvalues of P. If
the slope deviates significantly from one, proportionality is not
met, and therefore the null hypothesis of genetic drift can be
rejected.
In addition, advances in genotypeephenotype research in
pedigreed organisms have elucidated the genetic architecture
L. Schroeder and R.R. Ackermann
(including heritability and pleiotropic effects) underlying pheno-
typic diversity, focused mainly on dental variation (e.g., Hlusko
et al., 2004, 2006; Hlusko, 2016; Stojanowski et al., 2018, 2019;
Hardin, 2020, but see also Schluter, 1996). These quantitative ge-
netic studies have shown that certain phenotypic traits are genet-
ically correlated with others (e.g., characters in the dental arcade,
tooth size, body size), which has major implications for the
response of the phenotype to evolutionary pressures, but also for
the application of phylogenetic systematics; an approach that as-
sumes independent and uncorrelated characters (Hlusko et al.,
2006; Grieco et al., 2013). Furthermore, some research has also
found that this genetic patterning is conserved across multiple
mammalian taxa (e.g., Hlusko et al., 2011), which allows for
tentative application to human evolution (Brasil et al., 2020).
As is clear, these developments in the field of evolutionary
quantitative genetics have provided us with powerful tools for the
consideration of phenotypic evolutionary divergence in both
extant and extinct organisms, beyond the adaptationist paradigm.
Within this framework, one of the most important insights is that
divergence over time between species that happens through ge-
netic drift should be proportional to variation seen within species.
This is because divergence by genetic drift is essentially distrib-
uted randomly across the genome and phenotype, affecting all
traits roughly equally, while adaptive divergence deviates from
that pattern, with some regions diverging more or less than ex-
pected because they are being selected for or against. And
although there is a complex and sometimes opaque link between
the genotype and phenotype (as has been discussed in detail
elsewhere, e.g., Dowell et al., 2010; Milocco and Salazar-Ciudad,
2020; Aponte et al., 2021), as phenotypic variation in morpho-
logical characters resembles genetic variation (e.g., Cheverud,
1988; Hlusko, 2016), these quantitative genetic models and
predictions can be used to answer questions about pattern and
process in the human fossil record.
2.4. Applications of concepts, past and present
Over the past five decades, the analytical and theoretical ad-
vancements in evolutionary theory detailed earlierdespecially
those related to the hypothesis testing framework of quantitative
genetics, and the inclusion of nonadaptive process as an important
mechanism for morphological divergencedhave been widely
applied in the broader evolutionary biology literature (e.g.,
Lofsvold, 1988; Simon et al., 2016; Assis et al., 2017; Rossoni et al.,
2017; Machado et al., 2022), but have only recently been explic-
itly incorporated in studies of human evolution.
The first direct application of the Lande model to the hominin
fossil record came in 2004 when Ackermann and Cheverud applied
regression tests to assess the proportionality of between and within-
group facial variability across a number of hominin taxa, including
Australopithecus, Paranthropus, and early Homo. They found that
while genetic drift could be rejected for comparisons involving
Australopithecus and Paranthropus, with reconstructed selection
gradients indicating strong selection in the upper-face and zygo-
matic region, those involving early members of the genus Homo did
not deviate from expectations of neutrality (Ackermann and
Cheverud, 2004). Several subsequent studies have successfully
applied these techniques within the broader field of biological an-
thropology, including analyses of fossil hominins (see below), extant
primates (e.g., Marroig and Cheverud, 2004; Schroeder and von
Cramon-Taubadel, 2017; Schroeder et al., 2022), and recent
humans (e.g., Rolian et al., 2010; Smith, 2011; Savell et al., 2016;
Ponce de Leo n et al., 2018; Tran and Schroeder, 2021), demonstrating
the robustness of these techniques for our understanding of
5
Journal of Human Evolution 174 (2023) 103296
evolutionary process. Some of these studies have appeared in the
pages of JHE. Weaver et al. (2007) showed that the divergence be-
tween Neanderthals and recent humans in cranial morphology fol-
lowed a neutral pattern. Grabowski and Roseman (2015) used
selection gradients to determine the selection pressures acting on
hip morphology across a number of hominin taxa. Specifically, they
find evidence for fast rates of evolution and selection on a number of
traits in the transition from our last common ancestor with chim-
panzees (they use extant chimpanzees to model this) to Austral-
opithecus afarensis, from A. afarensis to Homo heidelbergensis, and
within later Homo. And finally, Schroeder and Ackermann (2017)
used a combination of approaches to assess the relative roles of
genetic drift and natural selection in the evolution of Homo skull
morphology, finding that genetic drift was widespread across much
of this diversification, especially in neurocranial morphology, but
that natural selection was important for certain aspects of
morphology related to mastication, particularly for the diversifica-
tion of the Dmanisi hominins from early Homo, and between Homo
rudolfensis and other early Homo groups (Schroeder and Ackermann,
2017). Interestingly, the divergence between Homo naledi and other
Homo groups seems to follow a neutral pattern.
A few additional studies outside of JHE have applied these
techniques to the hominin fossil record, focusing on Austral-
opithecus, Paranthropus, and the transition to early Homo.
Schroeder et al. (2014) applied a series of analyses based on
quantitative genetic theory to assess the evolutionary processes
underlying skull divergence between potential ancestral groups of
hominins. They found evidence for selection between Austral-
opithecus sediba, early Homo, and A. africanus, while transitions
from A. africanus to early Homo followed a neutral pattern
(Schroeder et al., 2014). Grabowski (2016) analyzed the evolution of
brain and body size in fossil hominins, two traits that have gener-
ally increased throughout our lineage. They find strong evidence for
selection on brain size during hominin evolution (last common
ancestoreA. afarensis, A. afarensiseH. erectus, H. erectuseH. hei-
delbergensis, H. heidelbergensiseH. sapiens), but not for body size.
This is interpreted as an effect of the covariation between these
traits, indicating that body size may not have been under direct
selection pressures during human evolution, but instead may have
increased because of correlated evolution with brain size
(Grabowski, 2016). Similarly, Diniz-Filho and Raia (2017) applied a
series of models derived from quantitative genetics to investigate
the evolution of brain and body size in Homo floresiensis, and to test
expectations of the Island Rule. Their results indicated a wide-
spread rejection of neutrality in both the evolution of brain and
body size in H. floresiensis from a putative H. erectus ancestor,
consistent with directional selection caused by insular dwarfism,
with stronger selection on brain size (Diniz-Filho and Raia, 2017).
Several studies by Baab (2018, 2021) have also used aspects of the
Lande model to assess cranial variation in the genus Homo, finding
evidence for neutral evolution underlying the divergence of a
number of taxa (similar to Schroeder and Ackermann, 2017), but
also that selection drove the diversification of the frontal bone in
H. erectus. Finally, Hlazo (2018) and Hlazo et al. (2018) identify
evidence of natural selection between Australopithecus and Para-
nthropus skulls, as well as between eastern and southern African
Paranthropus, while genetic drift could not be rejected for diver-
gence between Paranthropus taxa within eastern Africa (Para-
nthropus aethiopicus and Paranthropus boisei). Collectively, these
studies underscore the utility of this framework for teasing apart
evolutionary process, but also point to the importance of genetic
drift during human evolution. This is a significant finding, as
adaptive explanations have dominated the literature since Darwin,
including within the pages of JHE itself.
L. Schroeder and R.R. Ackermann
More specific genotypeephenotype quantitative genetic
approaches to the hominin fossil record have focused on applying
inferences from studies that have used pedigreed data to identify
the genetic patterning of certain phenotypic traits. For example,
Hlusko (2016) identified two ratios (molar module component and
premolaremolar module) describing phenotypic variation in
primate dentition that best reflect the underlying genetic archi-
tecture (i.e., are heritable with no pleiotropic effect), and hence can
be used to elucidate evolutionary histories and adaptive shifts
through time. They find that these ratios distinguish between
different hominin genera, potentially pointing to different adaptive
regimes. A follow-up study by Brasil et al. (2020) showed that the
molar module component was able to identify genus-level adaptive
shifts in hominins, while the premolaremolar module reflected
species-level differentiation, indicating that the latter may have
been more evolvable through time. In addition, there are several
studies that have incorporated specific model-bound approaches
for testing the congruence of neutral genetic variation (or
geographic distance from Sub-Saharan Africa as a proxy for neutral
genetic differentiation) and phenotypic variability as it applies to
recent human evolution. Many of these investigations have found
that a substantial number of traits across the skeleton in humans
have evolved neutrally (Hanihara et al., 2003; Relethford, 2004;
Roseman, 2004; Hanihara and Ishida, 2005; Harvati and Weaver,
2006; Manica et al., 2007; Hanihara, 2008; von Cramon-Taubadel
and Lycett, 2008; Betti et al., 2009, 2010; Smith, 2009; von
Cramon-Taubadel, 2009, 2010; Reyes-Centeno et al., 2017; Betti
and Manica, 2018; Rathmann and Reyes-Centeno, 2020). Like that
of the dental studies above, the results of this research have im-
plications for the use of certain traits in analyses, assuming that
those traits are reflective of the underlying genetic architecture.
In JHE, some additional phenotypic studies that have used
quantitative genetic approaches and neutral models of evolution
include those that have focused on heritability estimates (e.g.,
Hardin, 2020), G-matrix and P-matrix correlation (e.g., de Oliveira
et al., 2009), and those that have explicitly incorporated popula-
tion structure into their analyses (e.g., Betti et al., 2014); however,
none of these approaches, except for one twin-study used to esti-
mate the heritability of having higher average skin temperatures
during exposure to cold (Koertvelyessy and Thompson, 1975), are
reflected in the early days of the journal (1972e1977).1 Rather, what
we see is a disconnect between studies focused on genetics and
those focused on morphology, mostly due to the lack of a theo-
retical and analytical bridge between evolutionary process and the
phenotype, as well as the fact that Lande's quantitative genetic
phenotype-applicable model was only published in 1976.2
Regardless of these issues, many early papers did discuss
morphological evolution and process, usually within an adapta-
tionist framework, although some did include discussions of
genetic drift. Of those that did, we do find acknowledgment of the
theoretical developments of Kimura (1968) and King and Jukes
(1969), especially their work on mutation rate and the neutral
theory; however, this was mostly limited to genetic studies (e.g.,
1
Using Scopus, we searched for the terms ‘quantitative genetic/s,’ ‘genetic drift/
random drift/neutral evolution,’ ‘adaptation/adaptive/natural selection,’ and ‘heri-
tability’ in the 347 JHE articles from 1972 to 1977. ‘Genetic drift/random drift/
neutral evolution’ features 18 times, ‘adaptation’ features 77 times, ‘heritability’
features 4 times, and ‘quantitative genetics’ features once.
2
This is effectively captured in this quote by Jacquard (1977: 734) in JHE, “Finally
it is necessary to distinguish two separate fields: one deals with phenotypes, the
purpose is efficiency and the methods are statistics; the other deals with genotypes,
the purpose is understanding and the methods are probabilities. Between these
two fields, we must admit that, in the present state of science, the communications
are at least difficult.”
6
Journal of Human Evolution 174 (2023) 103296
Boyer et al., 1972; Kohne et al., 1972), with morphological studies
only considering genetic drift in a hypothetical sense. For example,
Gabow (1977) considers the evolution of brain size in hominins and
the possible action of genetic drift on small populations with
uneven gene flow. Although Gabow (1977) is distinct from others in
that it incorporates a range of evolutionary processes into a dis-
cussion of morphological divergence in human evolution, the
approach lacks proper hypothesis testing.
Two early papers focusing on evolutionary process, including
genetic drift, that provide an interesting comparison to current
applications of quantitative genetic theory are Bilsborough (1973,
1976). Using an approach proposed by Lerman (1965) to calculate
rates of evolution, Bilsborough estimated rates between various
hominin groups, including A. africanus, P. boisei, H. erectus, Ne-
anderthals, H. sapiens, and some Middle Pleistocene Homo
individuals, first only on a subset of cranial vault traits (1973), then
on a number of cranial modules and dental traits (1976). The
calculation that was used is based on the Mahalanobis' distance
(D) between two groups divided by divergence time
pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
( Dz0 P1 Dz=t). This measure is similar to Lande's estimate of
evolutionary rate, the generalized genetic distance (GGD) that we
introduced earlier, i.e., Nte Dz0 G1 Dz (Lande, 1979), which is essen-
tially a Mahalanobis' distance measure, squared, scaled in this
case by effective population size and divergence time. However,
unlike Lande's GGD, the application of Lerman's rate of evolution
does not allow for a detailed hypothesis testing approach to help
elucidate possible evolutionary processes like that offered by a
quantitative genetic framework. This can be seen in Bilsborough's
discussion of his results in both papers; he makes inferences
about strong selective pressures on cranial capacity and the
masticatory region; however, these are based on patterns of dif-
ferences in the magnitude of rates. Although Bilsborough's papers
(1973, 1976) stand out in their innovative approach to assessing
morphological variability, the consideration of gene exchange
between hominin groups, and what he terms ‘mosaic evolution’ as
it relates to differing patterns of cranial and dental morphological
change, the approach is limited in light of the potential of quan-
titative genetics.
2.5. Comparing methods: Rates of evolution
To compare the differences between the two approaches, we
used Lerman (1965) and Lande's GGD to calculate evolutionary
rates between a number of hominin groups for 14 cranial vault
traits based on 8 cranial landmarks (Table 1). Data for this analysis
were taken from previous studies (Schroeder, 2015; Schroeder and
Ackermann, 2017), and include KNM-ES 11693 (Middle Pleistocene
Homo ~200e400 ka; Br€ auer and Leakey, 1986), KNM-ER 406
(P. boisei ~1.7 Ma; McDougall and Brown, 2006), MLD 37/38
(A. africanus ~3.32e2.9 Ma; Latham and Herries, 2004), KNM-ER
3883 (H. erectus ~1.5 Ma; Lepre and Kent, 2015), and SAM-AP
4692, a H. sapiens individual from Peer's Cave in South Africa
(~7200 years old; Stynder et al., 2009), and a comparative sample of
86 recent African H. sapiens individuals from the Raymond A. Dart
Collection at the University of the Witwatersrand, and the Iziko
Museums of South Africa. We performed comparisons between
possible ancestoredescendent pairs, with individual hominin
specimens used to represent species/group means, and the
comparative human sample as our model of within-group covari-
ance (P-matrix), calculating both the GGD and the rate according to
Lerman (1965). As far as possible, comparisons mirrored those in
Bilsborough (1973). Several parameters had to be estimated for the
implementation of the GGD, including effective population size,
divergence times between species, and generation time. Although
L. Schroeder and R.R. Ackermann
Table 1
Landmark definitions for traits used in this study.a
Landmark abbreviation Landmark
AP Anterior pterion
POR Porion
MAS Mastoidale
PN Parietal notch
AST Asterion
LA Lambda
BR Bregma
IN Inferior nuchal
a
The 14 traits extracted from these landmarks are as follows: MASeAST, PNeMAS, ASTePOR, PNePOR, BReLA, INeLA, INeBR, PNeBR, PNeLA, ASTeLA, APeBR, APePN,
APePOR, and APeLA.
these parameters are integral to this approach, and errors in esti-
mation can have an effect on the eventual interpretation of results,
the GGD is based morphological difference and thus overall pat-
terns of rates will not be affected. More detail about this analysis
can be found in the Supplementary Online Material (SOM) S1.
Analyses were performed in R v. 4.1.0 (R Core Team, 2022).
Results are provided in Table 2. As expected, the findings of the
GGD analysis provide more detail to the comparisons between
hominin groups in cranial vault traits when compared to Lerman's
rate calculation, although the general pattern of rates is similar.
Three comparisons, A. africanus to H. erectus, H. erectus to Middle
Pleistocene Homo, and Middle Pleistocene Homo to H. sapiens,
show no departure from a neutral model in the GGD analysis,
indicating that genetic drift was likely at play in their divergence.
This result differs from the findings of Bilsborough (1973). For the
A. africanus to H. erectus and Middle Pleistocene Homo to
H. sapiens transitions, Bilsborough (1973) invokes the action of
selection as an explanation for the differentiation between these
groups, although rates of evolution may well have been inflated
because of the dates used in the calculations. For the H. erectus to
Middle Pleistocene Homo transition, Bilsborough does suggest
that the differences between the two are much more “econom-
ical” (Bilsborough, 1973: 397), and discusses the potential poly-
typic nature of H. erectus, as well as the possibility of gene
exchange between groups, i.e., “the contribution of each of several
possibly ancestral groups to the gene pool of a descendent pop-
ulation is directly proportional to the degree of morphological
resemblance to that descendent population.” (Bilsborough, 1973:
398). As for the remaining comparison, A. africanus to P. boisei, a
fast rate of evolution was detected in the GGD analysis; an indi-
cation of directional selection (Table 2). This comparison was also
included in Bilsborough (1973), and selection was proposed as a
driver for this transition.
Overall, although the pattern of rates is similar across the two
methods, the underlying quantitative genetic theory in the GGD
allowed for a more detailed differentiation of various evolutionary
processes using hypothesis testing. And while there are many
alternative methods that are available for understanding morpho-
logical change through time, such as phylogenetic comparative
methods (e.g., Go  mez-Robles et al., 2017), the framework of
evolutionary quantitative genetics provides a series of simple yet
powerful approaches that have advanced our understanding of the
complex, multiprocess morphological divergence in hominin evo-
lution, highlighting the prevalence of genetic drift in human
evolution.
7
Journal of Human Evolution 174 (2023) 103296
Landmark definition
The most anterior point on the sphenoparietal
suture/the intersection of the parietal, sphenoid and frontal bones
The most superior point on the margin of the external auditory meatus
The most inferolateral point on the mastoid process
The indentation or angle between the squamous and petrous parts of the
temporal bone, taken on the superior border of the squama temporalis
The junction of the lambdoid, parietomastoid and occipitomastoid sutures
The junction of the sagittal and lambdoid sutures, taken in the midline
The midline junction of the coronal and sagittal sutures
The most inferior midpoint on the inferior nuchal line
3. The influence of hybridization on human evolution
3.1. Historical developments
Hybridization refers to breeding between two distinct taxo-
nomic units (species, subspecies, or lineages; see e.g., Taylor and
Larson 2019). Experimental and comparative studies examining
the outcomes of hybridization and its implications for the viability
of taxa, morphological variation, and the expression of the
phenotype in an evolutionary context have a long history. More
than 150 years ago, Darwin explored the nature of species and
varieties in terms of their ability to interbreed, and its effect on size,
vigor and sterility, including demonstrating that mating between
species can be difficult (Darwin, 1859). Although mostly occupied
with the question of sterility and inheritance (Roberts, 1919), he
recognized the range of variation seen in hybrids, including non-
intermediate phenotypes: “There are certain hybrids which,
instead of having, as is usual, an intermediate character between
their two parents, always closely resemble one of them” (Darwin,
1859: 256). The basis of Mendel's work on inheritance was also
grounded in cross-breeding experiments, in this case among vari-
eties of one species, providing an understanding of the nature of
gene segregation and dominance (Mendel, 1866). Although works
such as these were not focused on the deep exploration of hy-
bridization and the effects of gene exchange as an evolutionary
force per se, they nonetheless illustrate how influential scientists
trying to understand evolution and its genetic underpinnings (and
in the absence of genetic data), including adaptation and specia-
tion, were well aware of the power genetic exchange has to provide
insight into the relationship between the genotype and phenotype.
In the first half of the 20th century, botanists and zoologists
exploring the effects of hybridization had divergent perspectives,
drawing disparate conclusions that shaped our understanding of its
importance in different ways (Taylor and Larson, 2019). For
example, botanist G.L. Stebbins considered hybridization to be a
creative force for generating genetic diversity (Stebbins, 1950), a
perspective that was quickly taken up across botany and has long
been widely accepted (Grant, 1981; Rieseberg, 1997; Arnold, 2015).
In contrast, zoologists such as T. Dobzhansky and E. Mayr portrayed
hybridization as rare among animals, and solely a negative selective
agent that reinforced species boundaries (Dobzhansky, 1937; Mayr,
1942), a perspective that persisted for many decades in animal
studies. Although hybridization can lead to decreased fitness in
some cases (e.g., Sage et al., 1986), this perspective minimized any
role of hybridization in generating novelty for selection to act on
L. Schroeder and R.R. Ackermann Journal of Human Evolution 174 (2023) 103296

(Barton, 2013). These different foci and perspectives likely had an

The 95% confidence interval for a chi-square distribution at 14 degrees of freedom is (5.63e26.1). GGD values that fall within this interval can be attributed to genetic drift, smaller values indicate stabilizing selection, and
Evolutionary

Genetic drift
Genetic drift
Genetic drift
impact historically on the consideration of the relevance of

Directional
processf

selection
hybridization to human evolution. The racialized implications of
applying hybridization studies to studying people (e.g., in the
context of the prevalent historical narrative of miscegenation; see
Anderson, 2012 and Caspari 2018 for an overview of its application
22.94
24.18
15.42
30.26
GGD

in early physical anthropology) may have also played a role.

size is estimated as 18,500 (Huff et al., 2010), and Homo sapiens is estimated at 13,600 (Henn et al., 2012). Comparisons include average effective population sizes for the two groups being compared.
From the latter part of the 20th century, however, there was a

Effective population size for early hominins (Australopithecus africanus and Paranthropus boisei) is estimated to be 21,000, based on a Pan model (Yu et al., 2004), fossil Homo effective population
growing (albeit not universal) consensus that hybridization has the
100,000 yearse

potential to be a creative force in many contexts, and it is now well-

D units per

(42.28)
Lerman's

(4.08)
(2.31)
(8.66)

established that hybridization has substantially impacted evolution

and speciation of both plants and animals (Anderson, 1953;
2.84
1.32
0.64
1.12

Stebbins, 1959; Rieseberg 1995; Barton, 2001; Mallet, 2007; Abbott

et al., 2013; Arnold, 2015). This includes in mammals, a substantial
The covariance matrix was multiplied by a heritability of 0.4 to take into account imperfect heritability of cranial traits. This estimate was taken from Roseman et al. (2010).

shift in the more than half-century since Stebbins (1959) pointed

2.26
0.62
0.26
0.46
Ne/t

out the dearth of hybridization studies of them. Research now

shows that hybridization is a frequent occurrence in nature,
Estimated effective

including between both closely and distantly related species

population sized

(Mallet, 2005; Mallet et al., 2016), and that the movement of alleles
16050
18500
19750
21000

into lineages can provide novelty that is selectively advantageous,

resulting in hybrid vigor (Grant et al., 2004; Dasmahapatra et al.,
2012; Kirkpatrick and Barrett, 2015; Hanot et al., 2019). Impor-
tantly, this body of research has overturned the historical narrative
of hybridization as solely rare and detrimental (e.g., Mayr, 1942).
corrected by generation

Alleles acquired through hybridization provide new variation (and

length (t in GGD)c
Divergence time

new genetic combinations) that may not have arisen through

29820.00
75480.00
45600.00

mutation alone. Critically, hybridization does not only facilitate

7100

adaptation through the injection of new variation and the subse-

quent action of natural selection, but can introduce genetic variants
that have a selective advantage, facilitating rapid change, though
establishing the adaptive function of introgressed genetic material
Divergence time was calculated as the difference between the estimated mid-point date for each species/group.

remains difficult (Taylor and Larson, 2019). Hybridization can also

introduce neutral variation into lineages, a potential resource for
Divergence time

Abbreviations: D ¼ Mahalanobis Distance; GGD ¼ generalized genetic distance; Ne ¼ Effective population size.
(t in Lerman)b

later evolutionary change. Understanding hybridization is therefore

177500
745500
1887000
1140000

a vital part of understanding the role of both adaptive and neutral

variation, potential drivers of divergence and speciation in human
Generation time is estimated at 25 years for a generalized great ape (Langergraber et al., 2012).

evolution.
Results of Lande's (1979) generalized genetic distance and Lerman's (1965) rates of evolution.

3.2. Model organisms as tools for understanding hybridization in

D2 corrected for

heritabilitya

human evolution
imperfect

10.15
38.97
58.93
65.70

At the time of JHE's establishment, there was very little empir-

ical research being done on hybridization in human evolution; the
research briefly highlighted above occurred within evolutionary
biology, at the time largely outside of the realm of biological
25.37
97.42
147.33
164.26
D2

anthropology. Most of the early JHE papers that considered hy-

Values from Bilsborough (1973) are indicated in parentheses.

bridization were case studies of primate hybrids in captivity and the

wild (e.g., Gijzen, 1973; Bernstein, 1974; Dunbar and Dunbar, 1974).
5.04
9.87
12.14
12.82

However, one JHE paper, in particular, stands out as an exception,

D

namely a theoretical exploration of the effect hybridization might

have had on human ancestors. Roberta Hall (1977) reviews the
Australopithecus africanuseParanthropus boisei

paleobiology and systematics of Canis lupus (wolf) and Canis latrans

(coyote) to develop a model for considering southern African Aus-
larger values indicate directional selection.
Middle Pleistocene HomoeHomo sapiens

Australopithecus africanuseHomo erectus

Homo erectuseMiddle Pleistocene Homo

tralopithecus (i.e., ‘robusts’ and ‘graciles’ as they were considered at

the time). She concludes that wolves/coyotes are ecologically/
behaviorally analogous, including in terms of their breadth of dis-
tribution, and therefore good models for considering variation
across these hominins (see also Hall, 1978). Hall then uses this to
argue that, like wolves and coyotes, A. africanus and Paranthropus
robustus are ‘good’ biological species that nonetheless would have
hybridized to form viable hybrid populations under the right
Comparison

circumstances, retaining distinctiveness at the species but not the

generic level (i.e., they were not different in kind). Although many
Table 2

of the details about Australopithecus and Paranthropus biology are

a

e
b

f
c
d

no longer correct (such as body size and dietary differences),

8
L. Schroeder and R.R. Ackermann
nonetheless the mere consideration of them being similarly
divergent, but able to hybridize, like wolves and coyotes was
exceptional within the field. In considering this topic, rather than
emphasizing species barriers, the author seriously questioned the
rigidity of species concepts and especially the biological species
concept as it applies to our evolution: “The concept “species” is a
concept and hence a tool of science; it is not a law of nature or a
Procrustean bed into which data must be forced at all costs” (Hall,
1977: 524). “Following the wolf-coyote model the existence of two
specific forms does not indicate that no inter-breeding occurred but
rather that if it did occur it was not sufficient to shatter the
ecological and morphological stability of the two groups” (Hall,
1977: 527).
Early approaches such as this laid the foundation for later work
including a more widely recognized reticulate model for our origins
based on analogs with baboons (Jolly, 2001). Jolly (2001) suggested
that Late Pleistocene human population structure was baboon-like,
with different species interfertile, albeit morphologically distinct,
and even speculated that humans might have acquired advanta-
geous traits from groups like Neanderthals, suppositions that have
turned out to be largely correct (see more below; Jolly, 2016).
More recent empirical studies examining patterns of skeletal
variation in animal models have extended this approach. These
studies have provided a way of illuminating population history,
understanding fitness, and potentially determining how selection
on genes introduced through gene exchange shapes the phenotype,
results of which can be applied to the human past. This research
shows that new variation, even novelty, is produced through
hybridization, and we can see it quite clearly in skeletons of
numerous animals, including coyote-wolf hybrids (Zdjelar et al.,
2021), baboons (Ackermann et al., 2006, 2014; Eichel and
Ackermann, 2016), other primates (Ackermann and Bishop, 2010;
Buck et al., 2021) and other mammals (Leamy, 1982; Thorpe and
Leamy, 1983; Ackermann et al., 2010; Warren et al., 2018; Hanot
et al., 2019). Baboons and canids represent particularly good ana-
logs for hominins in terms of being medium-sized land-based
mammals that are geographically widespread, as recognized by
Hall and Jolly (and others).
Studies of pedigreed baboon skulls (Ackermann et al., 2006,
2014; Eichel and Ackermann, 2016), have examined trait variation
in a captive sample of Anubis baboons (Papio anubis), yellow
baboons (Papio cynocephalus), and their hybrids. First-generation
(F1) hybrids in particular had a high frequency of supernumerary
teeth, especially distomolars, and displayed a pattern of expression
that differed from ‘normal’ trait variation. F1 hybridsdespecially
malesdalso have enlarged anterior nasal cavities (Eichel and
Ackermann, 2016) and are often large in size more generally,
resulting in increased variation overall. The frequency of atypical
suture morphology is also high in these hybrids. Importantly, these
dental and sutural traits persist into later generations, including
second-generation F2 (i.e., F1  F1) animals, backcrosses (B1), and
other recombinant generations (Ackermann et al., 2014), with
additional variants like reduced teeth and rotated teeth also
present, making this model more relevant to the fossil record
where we are likely to come across a variety of recombinants and
therefore considerable variation. Trait variation such as this is not
unique to baboons; supernumerary teeth are also present in both
recent and late Pleistocene ground-squirrel hybrids (Goodwin,
1998), with a pattern of expression that is rare for nonhybrid
ground squirrels. A confirmed first-generation male beluga/
narwhal hybrid lacks a tusk (actually a tooth), with atypical
mandibular teeth unlike what is seen in either parent (Heide-
Jørgensen and Reeves, 1993; Skovrind et al., 2019), while both
dental and horn anomalies are present in hybrid wildebeest
(Ackermann et al., 2010). Like baboons, mice also show relatively
9
Journal of Human Evolution 174 (2023) 103296
large size in hybrids, and also skull shape that is somewhat trans-
gressive relative to their nonhybridized parents (Warren et al.,
2018). Finally, a recent study of coyote-wolf hybrids also showed
a high frequency of dental anomalies, dental crowding, and sutural
anomalies (Zdjelar et al., 2021), providing further support that
these types of traits are indicative of hybridization across a wide
range of mammals.
When lineages/subspecies/species hybridize, the parental
groups potentially have different co-adapted gene complexes. In
this context, studies of hybridization in model organisms have
provided insight into the genetic architecture of quantitative and
behavioral traits, as well as the effect that hybridization can have on
the evolvability of traits (e.g., Gillespie et al., 2020). Mouse crosses
have revealed pleiotropic effects on mandibular morphology
(Klingenberg et al., 2004), and specific quantitative trait loci related
to long bone length (Norgard et al., 2009). Research on threespine
stickleback fish has been particularly valuable for elucidating the
role of hybridization in contributing standing genetic variation for
rapid adaptation (e.g., Schluter and Conte, 2009; Galloway et al.,
2020; Reid et al., 2021). Similar patterns have been revealed in
canids, with a number of positively selected genes associated with
morphology and behavior introduced through hybridization (e.g.,
Kays et al., 2010; vonHoldt et al., 2010; Pilot et al., 2021).
Examining patterns of variation when they come together, as
above, therefore gives us direct insight into underlying genetic ar-
chitecture (however, this can also lead to epistatic effects which are
challenging to map, e.g., Mackay, 2014). Developmental anomalies
associated with, e.g., tooth formation, point to divergence in the
genes responsible for this trait and may affect seemingly unrelated
traits due to pleiotropy. The novel dental and sutural variation we
observe in hybrid mammals appears to be minor enough that it
does not affect the fitness of individuals (Ackermann et al., 2014).
Based on the information generated from these model organ-
isms, it has been possible to identify evidence for hybridization
(which includes possible F1 and later-generation hybrids) in the
human fossil record.3 This includes evidence for interbreeding
between Neanderthals and early humans, in the form of both
atypical dental variation, as well as a wide range of variation more
generally (Ackermann, 2010; Harvati and Ackermann, 2022). Homo
sapiens specimens like Oase I and Oase II have been argued to be
hybrids based on morphology, including their large size and third
molar megadontia (Ackermann, 2010; Trinkaus et al., 2013;
Trinkaus, 2018), and their DNA has confirmed percentages of the
genome derived from Neanderthals that indicate relatively recent
ancestry (9.90% for Oase I and 6.06% for Oase II; Fu et al., 2015;
Siska, 2019). Several other late Middle to Late Pleistocene speci-
mens, including but not limited to Skhul IV and V, Amud 1, Cro
Magnon 3, Pavlov 1, Mlade c 5, and individuals from Qafzeh, may
also have morphology consistent with hybridization (Ackermann,
2010; Harvati and Ackermann 2022), a hypothesis that requires
further testing. There is also some evidence that A. afarensis spec-
imens from eastern Africa may have hybridized, presumably with
other taxa living in relative proximity at the same time, as shown by
the presence of left mandibular fourth molar roots in the corpus of
A.L. 198-1 (White and Johanson, 1982; Ackermann, 2010). Austral-
opithecus afarensis is also known to be highly variable (e.g., Kimbel
and Delezene, 2009), which is consistent with our expectations
from our hybrid mammal models. There is also possible evidence
3
It should also be stated here that while there are other approaches that can be
used to understand the role of past gene flow and migration between groups (e.g.,
Relethford and Blangero, 1990; Weaver, 2018), many of these approaches are reliant
on either genetic data, or large sample sizes for the estimation of within-group
covariance, both of which are unfortunately lacking for the fossil record.
L. Schroeder and R.R. Ackermann Journal of Human Evolution 174 (2023) 103296

for hybridization in H. floresiensis from the island of Flores,
Indonesia, in the form of atypical bilaterally rotated premolars
(Ackermann, 2010).
Returning to Hall's (1977) hypothesis, although many of the
details of the paper are no longer correct, given our current
understanding of Australopithecus and Paranthropus diversity and
phylogeny, we can still examine whether this variation, and spe-
cifically the variation within and differences between A. africanus
and P. robustus, is consistent with data from model organisms,
especially canids. To date, only one individual specimen from these
hominin taxa shows evidence for dental or sutural anomalies,
P. robustus cranium SK 83 from Swartkrans, which has a supernu-
merary lateral incisor in the right maxilla (Ripamonti et al., 1999).
Because maxillary incisors are the most common type of super-
numerary tooth (Lavelle and Moore, 1973; Rajab and Hamdan,
2002), and unlike distomolars, are not what is seen in the studies
of model organisms described above, this is not strong evidence for
hybridization. To further explore the possibility of hybridization
between these taxa, and the hybrid status of SK 83 in particular, we
performed a PCA of maxillary morphology for C. latrans (n ¼ 20),
C. lupus (n ¼ 20) and their hybrids, C. latrans var. (n ¼ 20; Fig. 2A),
and for P. robustus (n ¼ 7) and A. africanus (n ¼ 4; Fig. 2B). Data were
taken from previous studies (Schroeder, 2015; Zdjelar et al., 2021),
analyses were performed in PAST v. 4.09 (Hammer et al., 2001), and
details of the analysis can be found in SOM S2 and SOM
Tables S1eS4. Our expectation based on the canid data is that
hybrids will be intermediate to parents (Zdjelar et al., 2021), with
some individuals that are transgressive (outside of the range of the
parent taxa), a result consistent with previous analyses of both
baboon species (Ackermann et al., 2016) and mouse subspecies
(Warren et al., 2018). This is depicted in Figure 2A, where C. lupus
occupies the negative extreme of PC1 and PC2, C. latrans occupies
the positive extreme, with the hybrids falling in between. In our
hominin analysis, A. africanus and P. robustus are distinct morpho-
logically, while SK 83 is intermediate and transgressive relative to
both (Fig. 2B). This supports the possibility of hybrid status for SK
83, as does its extreme size, the largest in the sample (SOM
Table S4), though obviously this hypothesis remains to be tested
further. Clearly, our current evidence drawn from animal models
has improved our ability to answer the kinds of questions being
asked by Hall (1977). Finally, it is also worth noting that the
divergence time of the grey wolf and coyote is approximately 50 ka
(vonHoldt et al., 2016), which may make them even better models
for considering recently diverged taxa rather than deeply divergent
ones. Indeed, as argued elsewhere (i.e., Ackermann et al., 2019), the
persistence of ancient allele variants acquired through hybridiza-
tion (e.g., with Neanderthals, Denisovans) in humans living today,
especially those related to skin and other factors related to keratin,
immunity and high-altitude adaptations (as discussed further
below), is in striking parallel to what we see in canids.
In addition to the identifications above based on empirical evi-
dence drawn from model organisms, hybrid individuals have also
been proposed in the human fossil record based on other aspects of
their morphology, like Lagar Velho 1 (Duarte et al., 1999; Bayle
et al., 2010), Cioclovina 1 (Soficaru et al., 2006), Vindija (Smith
et al., 2015), especially for intermediate or mosaic phenotypes,
although the hybrid status of many of these specimens has been
considered inconclusive (Klein, 2003, 2009) or actively disputed
(Tattersall and Schwartz, 1999; Harvati et al., 2007; Stringer, 2012).
Nevertheless, as a whole, we now have substantial morphological
evidence that contemporaneous hominin taxa were interbreeding.
However, there is still a considerable amount of work to be done on
the phenotype, as will be discussed further below.
3.3. Genetic evidence and the hybrid phenotype in human evolution
In addition to phenotypic evidence, we also have consid-
erabledand ever-growingdgenetic evidence for hybridization
between post-1 Ma lineages in human evolution, the period rele-
vant to the origin of our species, H. sapiens. This genetic evidence
has been well-described elsewhere (e.g., Ackermann et al., 2016;
Dannemann and Racimo, 2018; Ackermann et al., 2019; Gokcumen,
2020), and includes evidence for movement of gene variants from
Neanderthals into early humans (Green et al., 2010; Fu et al., 2014,
2015; Villanea and Schraiber, 2019; Hajdinjak et al., 2021; Prüfer
et al., 2021), and vice versa (Kuhlwilm et al., 2016; Posth et al.,
2017; Chen et al., 2020), from Denisovans into early humans
(Reich et al., 2010; Meyer et al., 2012), and from both Neanderthals

Figure 2. Principal component (PC1 vs. PC2) plots of nine maxillary traits in: A) Canis lupus (n ¼ 20; green), Canis latrans (n ¼ 20; yellow), and their hybrids, C. latrans var. (n ¼ 20;
orange); B) Australopithecus africanus (n ¼ 4; grey) and Paranthropus robustus (n ¼ 7; purple) individuals. In panel A, the PCA plot of canids shows an intermediate position for the
hybrids, with the parental taxa being relatively differentiated in shape space. In panel B, the PCA plot of P. robustus and A. africanus shows separation between the two taxa. SK 83
falls outside of both convex hulls. Further detail of each analysis is provided in SOM S2 and Tables S1eS4. All individuals are scaled by their geometric means to reduce the effects of
size variation on the analysis. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article).

10
L. Schroeder and R.R. Ackermann
(Prüfer et al., 2014; Slon et al., 2018) and some unknown hominin
(Prüfer et al., 2014) into Denisovans. It also includes evidence for a
first-generation child of a Neanderthal mother and a Denisovan
father (Slon et al., 2018), and for genetic exchanges between ancient
and recent lineages in Africa (Hammer et al., 2011; Lachance et al.,
2012; Chen et al., 2020; Durvasula and Sankararaman, 2020; Lipson
et al., 2020; Wang et al., 2020). Given the growing number of in-
dividuals and taxa for whom ancient hybridization has been
documented, well beyond just hominins (Arnold, 2015; Taylor and
Larson, 2019), it seems likely that additional studies will continue
to increase evidence of gene exchange in our past. We do not,
however, have comparable genetic evidence for interbreeding
among earlier hominins, including all of those outside of our genus,
given current limitations around the preservation and methodo-
logical capabilities of ancient DNA research. That information is
only available from phenotypic studies such as those discussed
above (but see Popadin et al., 2022).
This paleogenomic research on human origins has allowed us to
explore how gene exchange among taxa has shaped phenotypic
variation in humans living today, providing a fuller understanding
of the nature of any adaptive benefit or harm as it relates to envi-
ronmental and cultural factors. Specifically, many of the genes
acquired in humans living today through ancient introgression are
related to skin/hair/keratin characteristics (Sankararaman et al.,
2014; Vernot and Akey, 2014; Dannemann and Kelso, 2017), im-
munity (Abi-Rached et al., 2011; Dannemann et al., 2016), lipid
metabolism (Khrameeva et al., 2014), and adaptation to extreme
environments (Huerta-S anchez et al., 2014; Hu et al., 2015; Racimo
et al., 2015; Hackinger et al., 2016). To expand on some of this
research, studies screening for Neanderthal haplotypes in human
genome databases have consistently found evidence for adaptive
introgression from Neanderthals into humans related to skin and
hair phenotypes, including alleles for hair color and skin pigmen-
tation levels (Vernot and Akey, 2014; Dannemann and Kelso, 2017).
In terms of immunity and adaptation to extreme environments,
there is evidence that both Denisovan and Neanderthal archaic
haplotypes associated with altitude adaptation, toll-like receptors
as they relate to innate immunity, and lipid metabolic processes
possibly in relation to diet, have been positively selected in humans
through adaptive introgression (Khrameeva et al., 2014; Racimo
et al., 2015; Dannemann et al., 2016; Hackinger et al., 2016). Over-
all, these studies suggest that as humans were leaving Africa,
positive selection of alleles introduced through hybridization may
have facilitated the range expansion for our species, which is also
consistent with a recent review of the literature that shows that the
most common positive consequence of hybridization is the gain of
adaptive variation (Adavoudi and Pilot, 2022). The persistence of
acquired traits in living people, including some that are not bene-
ficial today (Sankararaman et al., 2014; Simonti et al., 2016; Mozzi
et al., 2017), further indicates that they were beneficial or mini-
mally neutral with respect to fitness in the past, unlike the larger
proportion of genes that were rapidly eliminated from the gene
pool (Juric et al., 2016; Petr et al., 2019).
Importantly, under the now-unsupported replacement model of
human origins, where people migrated out of Africa and
outcompeted and/or killed off other groups living in Europe and
Asia, we would likely not observe the full range of genetic and
phenotypic diversity that we see on the planet today. In this model
with no hybridization, the novel traits we see today that resulted
from genetic exchange would instead have had to evolve through a
long process of random mutation and selection over generations,
which may or may not have happened successfully, in the same
manner, or in the same timeframe as what occurred due to the
rapid acquisition of such traits through hybridization. Implicit in
the replacement model was the idea that the migrants had a
11
Journal of Human Evolution 174 (2023) 103296
competitive advantage, a narrative that has not held up under a
model that includes the acquisition of advantageous traits from
local people, and that is also not consistent with our current un-
derstanding of the cultural sophisticationdin both behavior and
material culturedof archaic groups (Sykes, 2020).
Hybridization among recent hominin taxa has had a lasting
impact on human evolution, with its genetic effects remaining a
proportionately small but geographically widespread part of
human diversity today. Both phenotypic and genetic data are
informative in understanding those dynamics and additionally can
provide links between genotype and phenotype (Brand et al.,
2022). However, we still have very little information linking
genotype to phenotype, especially in traits of interest to paleoan-
thropologists, such as traits that are taxonomically relevant or
those of known (adaptive) function. This is an easier task for single
loci of large (known) effect on morphology than for multigene
traits, but the latter characterizes most of our traits of interest in
human evolution. However, two recent studies examine
Neanderthal-derived gene variants in living European people as
they relate to cranial/brain form. Gunz et al. (2019) found a link
between Neanderthal gene variants and reduced endocranial
globularity for three regions of the genome, while Gregory et al.
(2017) found that degree of Neanderthal ancestry was associated
with Neanderthal-like shape variation in cranial form and brain
structure. Both of these studies highlight the multigene nature of
cranial form, and also point to ways in which we can understand
the underlying genetic architecture responsible for morphological
change through time.
4. The link between pattern and process: future
considerations
As we have outlined earlier, over the past 50 years, advances in
numerous fields such as evolutionary quantitative genetics and
ancient DNA, as well as the recognition of the prevalence of genetic
drift and gene exchange in human evolution, have provided our
discipline with a deeper understanding of the link between
morphological variation and evolutionary process outside of an
adaptationist paradigm. However, there are many avenues of
research in these domains that remain to be explored, especially as,
despite the increasing evidence for hybridization in human evolu-
tion and its importance, there is still fairly limited empirical
research on this question outside of the genetics literature. A
literature search comparing early and recent years of JHE publica-
tions indicates that references to hybridization and related terms
have not increased meaningfully in 50 years.4 Similarly, although
there has been a substantial increase in the use of quantitative
genetic approaches for understanding the relative roles of genetic
drift and natural selection in hominin evolution, especially with the
recent development of statistical toolkits, such as the recently
developed R package ‘EvolQG’ v. 0.2-9 by Melo et al. (2016), there
are still several promising avenues for future research and meth-
odological development. Below, we detail several research foci that
in our opinion have the potential to enhance our understanding of
evolutionary process, including the underexplored intersecting
nature of these processes, and further illuminate the demographic
history of hominins.
4
Using Scopus, we searched for the terms ‘hybridization,’ ‘hybridisation,’ ‘gene
flow,’ ‘introgression,’ ‘hybrid,’ or ‘reticulation/reticulate evolution,’ in the 347 JHE
articles from 1972 to 1977. Of 347 articles, 25 included at least one of these terms
(~7%). We did the same thing for the 683 JHE articles from 2016 to 2021, and found
only a slight relative increase: 56 articles out of 683 (~8%).
L. Schroeder and R.R. Ackermann
First, we believe that further studies that illuminate the links
between the genotype and phenotype (e.g., Gregory et al., 2017;
Gunz et al., 2019) will provide important insight into whether the
morphological changes that occur as a result of hybridization are
neutral or adaptive. We also need to test morphology, in addition to
genes, to understand this relationship, using methodological ap-
proaches such as those developed in quantitative evolutionary
genetics, especially those that can detect signatures of positive
selection in morphology. Importantly, a recent literature review of
hybridization across mammals demonstrated that while negative
consequences of hybridization appear to be more common than
positive or neutral ones, positive outcomes are typically harder to
demonstrate than negative ones and therefore may be under-
represented in the literature (Adavoudi and Pilot, 2022). In this
light, we need both to intensify focus on identifying positive
outcomes, and also to critically examine narratives of human
origins that continue to be shaped in ways that minimize the
importance of hybridization by pointing out that it is rare and
frequently detrimental. This drumbeat hearkens back to historical
perspectives (e.g., Mayr, 1942) and is inconsistent with the deep
and broad literature within organismal biology that highlights
hybridization's creative potential.
Second, one important aspect of quantitative genetic theory and
the Lande model that has been underexplored relates to how
genetic architecture, and especially the resultant covariation
among phenotypic traits, can facilitate or constrain the ability of
selection to operate. This is related to the concept of morphological
integration, referring to patterns of coordinated covariance be-
tween traits, and is also intrinsically linked to the concept of
modularity, which describes the apportionment of certain traits
into highly integrated functional/developmental modules that are
relatively independent of other such modules (Olson and Miller,
1999). As mentioned earlier, according to the Lande equation if
traits are highly integrated, then they are constrained to follow a
similar pattern of directional response to selection; some traits will
therefore respond even if they are not being directly selected for
(Lande, 1979). This is an especially important point to consider
when reconstructing phylogenetic relationships through evolu-
tionary time using cladistics, given that cladistic analyses are reliant
on trait independence (Mishler, 1994). We are not the first to point
this out.5 Hlusko (2004) outlined several issues plaguing paleon-
tological research, as well as several incorrect presumptions that
permeate the literature, including trait independence, the adaptive
importance of all traits, and the uniform and slow evolvability of
traits. Although there have been developments on this front using
pedigreed organisms, especially as it pertains to dental variation
(see Hlusko, 2016 for an overview), these approaches rely on
genetic data. One approach from evolutionary quantitative genetics
that can contribute to the solution of these issues when only
considering phenotypic data from fossil hominins is the recon-
struction of selection gradients (Lande and Arnold, 1983;
Ackermann and Cheverud, 2004; Marroig and Cheverud, 2005;
Schroeder and Ackermann, 2017; Schroeder and von Cramon-
Taubadel, 2017). As a reminder, the equation: b ¼ P1 s, describes
the selection gradient as a function of the inverse of the phenotypic
variance/covariance matrix of the traits in question, and the
differences between trait means before and after selection. If
morphological traits covary significantly, there may be a mismatch
5
Darwin's theory of the ‘correlation of growth’ refers to instances of constraints
due to trait covariation as a result of growth and development (Darwin, 1859).
Gould and Lewontin expand on this in their critique of the adaptationist program,
referring to traits that are by-products of selection elsewhere as a ‘spandrel’ (Gould
and Lewontin, 1979).
12
Journal of Human Evolution 174 (2023) 103296
in the direction of selection and response to that selection, resulting
in instances of indirect selection. As selection gradients represent
partial regression coefficients of traits on fitness, these traits
therefore do not confer a fitness benefit. This approach can there-
fore identify traits that are not under selection, and those that are
under indirect selection, i.e., correlated with other traits (such traits
should be avoided in cladistic analyses).
To demonstrate the utility of this approach, using the same data
from our rates of evolution analysis, and focusing on the compar-
ison between A. africanus and P. boisei, we reconstruct the direc-
tional selection gradient for this transition following the approach
in Lande and Arnold (1983). A detailed summary of the analysis is
provided in SOM S3 and SOM Table S5. Analyses were performed in
R v. 4.1.0 (R Core Team, 2022). Results depicted in Figure 3 show
that of the 14 cranial vault traits, nine selection coefficients are
significantly different from zero (confidence intervals do not
overlap with zero), with four of these showing evidence for indirect
selection, i.e., the trait response is in the opposite direction of the
selection pressure. Interestingly, parietal bone height (APeBR,
PNeBR; see Table 1 for the definition of landmark abbreviations)
seems to be under correlated selection, potentially for superior
parietal length (BReLA; Table 1).
Third, there is also a need to investigate whether and how
hybridization breaks down or relaxes patterns of morphological
integration in hominins, and what impact this has on the evolu-
tionary trajectory of taxa (e.g., Willmore et al., 2009; Nagendran
and Schroeder, 2022). Hybridization and introgression often
result in the recombination of genes in linkage, which results in a
decrease in integration between functionally/developmentally
related traits, and therefore examining integration in hybrids can
provide insight into genetic architecture, especially whether inte-
gration is produced by pleiotropic genes or genes in linkage.
Fourth, there has been little consideration of how hybridization
affects our phylogenies and interpretation of diversity, which has
both practical and conceptual implications, including both the fact
that phylogenetic trees do not take gene exchange into account and
theoretical concerns around how we divide species. We also believe
that the focus on adaptive (rather than chance) divergence has
Figure 3. A visual representation of significant selection coefficients necessary to
produce observed differences in cranial vault morphology between Australopithecus
africanus and Paranthropus boisei. Traits under direct selection (five traits: BReLA,
PNePOR, ASTeLA, ASTePOR, and APePOR) are presented by a solid line, whereas
those under indirect selection (four traits: APePN, PNeBR, APeLA, and APeBR) are
presented by a dashed line. Traits that are not under significant selection are not
shown (five traits: MASeAST, PNeMAS, INeLA, INeBR, and PNeLA); however, these
traits are also likely displaying responses that are due to correlation between traits. 3D
scan shown is A. africanus specimen MLD 37/38 in the foreground (in gray) super-
imposed on Sts 5 (in orange). Landmark abbreviation descriptions are provided in
Table 1. (For interpretation of the references to color in this figure legend, the reader is
referred to the Web version of this article).
L. Schroeder and R.R. Ackermann
served to reify the significance of species differences, and the notion
that some are more fit than others. In this context, the speciose
picture shown in Figure 1B, with distinct, discrete taxa, is not
consistent with the biological reality discussed here, where species
boundaries are fluid and lineages anastomose. As Hall (1977)
pointed out, the species concept is a tool of science, and we need
to align our taxonomy, narratives and physical depictions of human
evolution with our current understanding of how species diverge.
Fifth, Seehausen (2004) theorized a role for hybridization in
adaptive radiations, and recent studies of African cichlids and gue-
nons have suggested that hybrid swarms can provide the genetic
novelty for adaptive radiations (Parsons et al., 2011; Detwiler, 2019).
A recent review has also shown widespread genomic evidence for
hybridization in systems that have undergone adaptive radiations
(Berner and Salzburger, 2015). Although we do not currently have
concrete evidence for adaptive radiations in hominins, they certainly
exist in the evolutionary history of primates (e.g., Marroig and
Cheverud, 2005; Aristide et al., 2015; Harrison, 2016; Schroeder
et al., 2022), and this is a rich area for further investigation.
Sixth, another avenue of research that has been underexplored is
the application of these approaches to postcranial remains. With re-
gard to hybridization, most of the work described above on the
skeletal effects of hybridization has focused on crania. There have
been several previous studies on mice and primates indicating that
hybrids generally exhibit longer limbs and increased body size rela-
tive to their parent taxa (e.g., Carmon, 1963; Leamy, 1982; Thorpe and
Leamy, 1983; Leamy, 1992; Kurnianto et al., 1999; Kohn et al., 2001;
Warren et al., 2018), but these studies have only rarely looked at shape
variation in detail and have generally not been approached with an
eye toward interpreting questions relevant to hominin evolution. An
exception to this is a recent study by Buck et al. (2021) on hybrid
macaques, which investigated variation in the pelvis, and showed that
the effects of hybridization, in this case, are relatively small, possibly
because the parent taxa are themselves quite similar morphologically,
or due to developmental/functional constraints. Future research
needs to explore how hybridization affects shape variation in post-
crania with a lens toward interpreting key changes in the hominin
past such as those related to locomotion or childbirth.
Similarly, while we do have a few examples of quantitative
genetic studies that have used postcranial data (e.g., Grabowski and
Roseman, 2015 on hip morphology, Rolian et al., 2010 on the evo-
lution of human hands and feet, and Savell et al., 2016 on limb
lengths in recent humans), the vast majority have focused on skull
morphology. As mentioned earlier, this focus is in part related to the
disproportionate recovery of cranial, mandibular, and dental fossil
remains compared to postcranial elements, but also due to the
emphasis on skull morphology for differentiating between taxo-
nomic groups, which follows from the presumption that post-
cranial elements, with their intrinsic functionality, may not be as
taxonomically informative (McHenry and Brown, 2008). The
inclusion of more assessments of postcranial elements within a
quantitative genetic framework will allow for a deeper under-
standing of the connection between function and natural selection.
Finally, there have been several recent suggestions that some of
the skeletal anomalies seen in the human fossil record result from
inbreeding (Trinkaus, 2018; Ríos et al., 2019). Evidence from pri-
mates suggests that morphological traits indicative of inbreeding
include reduced size, anencephaly, polydactyly, syndactyly, and
limb malformations (Rawlins and Kessler, 1983; Chalifoux and
Elliott, 1986; Nakamichi et al., 1997; Charpentier et al., 2007; van
der Valk et al., 2019). In contrast, the evidence to date from
primates and other mammals, discussed earlier, indicates that hy-
bridization results in increased size and extremely rare dental and
sutural traits, in the absence of other associated diseases or
syndromes. However, traits such as atypical dentition do occur in
13
Journal of Human Evolution 174 (2023) 103296
individuals who are pathological in other respects, and further
empirical research that more clearly delineates expectations for
morphological variation under these different scenar-
iosdespecially in terms of distinguishing hybridization from
inbreedingdwill provide considerable insight into population
dynamics. Scenarios of small population sizes, with associated
isolation and expansion/dispersals, suggest that both will be causal
factors in shaping anatomical variation in the past.
5. Final thoughts on the science, society, and scientists
We wish to emphasize that while there has historically been an
adaptationist perspective to the study of morphological change
through time in human evolution, it is now clear that the evolu-
tionary forces of selection, gene exchange, genetic drift, and
mutation have all played a role in our diversification, as highlighted
in Figure 4. As has been discussed elsewhere, strict adaptationist
thinking does a disservice to understanding the complexity of
evolution (Gould and Lewontin, 1979; Koonin, 2016; Kissel and
Fuentes, 2021), but through methodological, conceptual, and
theoretical advances over the last 50 years, we believe that our
discipline is ready for a new paradigm. This new paradigm includes
a thorough consideration of all four forces, and should also focus on
how these forces work together to produce variation. For example,
because genetic change over evolutionary time frames occurs
predominantly through neutral processes (Kimura, 1968, 1991), it is
to be expected that drift would play a major role in shaping the
phenotype, and would be particularly powerful in small, mobile,
relatively isolated communities like we had in the deep past. Like
selection, genetic drift structures populations into distinct lineages,
and may have played a large role in diversification throughout
hominin evolution. Hybridization, in turn, occurs between these
distinct lineages, and while it can play an important role in keeping
taxa cohesive and groups evolving together, as discussed here it can
also lead to evolutionary innovation, including the rapid produc-
tion of novel and diverse genetic and phenotypic outcomes.
Hybridization can result in the transfer/acquisition of neutral
variation, but can be a particularly powerful force in combination
with selection if new phenotypic outcomes influence fitness, being
either adaptive or maladaptive (Ackermann et al., 2019; Taylor and
Larson, 2019). Where selection has acted to differentiate lineages,
hybridization may lead to very different outcomes than it does
where genetic drift has done so, given that the latter by definition
does not involve the evolution of differently coadapted gene com-
plexes, making the understanding of the relative roles of selection
and drift key to our understanding of the outcomes of hybridiza-
tion, and vice versa. By understanding this interplay among the
evolutionary forces, we can gain insight into population dynamics
that further informs our understanding of the past, yet such an
integrated approach has yet to be well-considered in models of
human evolution.6 Future research into the phenotype that ad-
dresses this complexity in understanding variation and evolution,
and the connection between genotype and phenotype, is essential.
We began this article by highlighting how hominin variation has
historically been studied within a typological framework, as a means
for classifying rather than an entrance into understanding complex
6
Using Scopus, we searched for any JHE articles in the 1972e1977 period and the
2016e2021 period that contained mention of a combination of the following terms,
grouped into three concept categories: (‘hybridization’ or ‘hybridisation’ or ‘gene
flow’ or ‘reticulate evolution’ or ‘reticulation’ or ‘introgression’ or ‘hybrid’) and
(‘random drift’ or ‘genetic drift’ or ‘non-adaptive’ or ‘neutral evolution’ or ‘drift’)
and (‘natural selection’ or ‘adaptation’). Between 1972 and 1977, there were 2 ar-
ticles out of 347 that made mention of any combination of terms in the three
concept groups, whereas between 2016 and 2021, there were 10 articles out of 683.
L. Schroeder and R.R. Ackermann Journal of Human Evolution 174 (2023) 103296

Figure 4. Schematic depicting our current cranial, mandibular, and dental phenotypic evidence for the combined action of genetic drift (yellow ellipses), gene flow (orange ellipses),
and selection (purple ellipses) in the hominin fossil record, based on the quantitative, variation-centered methodological approaches reviewed in this paper. Note that genetic drift
and gene exchange have been shown to be major players in structuring hominin diversity in the last million years, while selection is a major player across lineages ca. 2 Ma. Before
this, we have evidence for drift and possibly gene exchange; however, many of the taxa have yet to be examined using these approaches. Only results of multivariate trait analyses
are shown. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article).

process, and how, in some cases, these approaches have resulted in a
historical legacy that otherizes some and elevates others (Wolpoff
and Caspari, 2000; Athreya and Ackermann, 2020; Athreya and
Hopkins, 2021). For the ‘modern human origins’ narrative in
particular, an adaptationist model where one group was adaptively
superior to another and outcompeted them has resulted in the
historical marginalization of Asian taxa and researchers, and ironi-
cally (despite the ‘Out of Africa’ focus) in the primitivizing and
alienation of African ones (Athreya and Ackermann 2020). A more
nuanced postadaptationist framework allows us the opportunity to
reflect on how we language the past, and the implications of that for
people in the present, but it will need to be approached with care and
caution. This framework includes a few key messages. First, a lot of
the variation we see in the past (and present) is the result of chance,
not meaningful (in terms of fitness) adaptive differences. Second,
humans and our ancestors have a deep history of migration, inter-
action, and exchange, both within and outside of Africa. Indeed, it is
our ancestors coming together and exchanging genesdsome of
which were neutral but some of which conferred adaptive bene-
fitsdthat facilitated our success as a species by combining traits in
new ways. Finally, this history of migration and gene exchange
means that we are not easily parceled into discrete units. These are
all important lessons in today's world, providing evidence that can
be used to refute the biological basis of meaningful difference, race,
and othering, in contrast to the historically prevalent narratives of
dominance, superiority, and extinction.
Finally, while considering our mandate for this manuscript, i.e.,
to reflect on the history of our topic (especially within JHE) and
where the field is or should be going in the future, perhaps because
we (L.S. and R.R.A.) are women who are either from or currently
living in South Africa, we became acutely aware that much of the
history relayed above reads as a series of important discoveries by
remarkable (largely Western) men. This demographic is also re-
flected in the early papers in JHE, as were very different authorship

14
L. Schroeder and R.R. Ackermann Journal of Human Evolution 174 (2023) 103296

practices, and we asked ourselves whether and to what extent such

demographics have shifted over the lifetime of the journal as the
scientific endeavor has matured. These are important consider-
ations given that the identity and socio-political context of
researchers can shape the narrative direction of the journal and the
science itself (e.g., Athreya and Ackermann, 2020), an issue that is
relevant for JHE going forward.7
Figure 5 provides three infographics, the first looking at data
from the first six years of JHE's outputs, from 1972 to 1977, the
second from the six years immediately following the shift in
editorial oversight to include the USA, from 1986 to 1991, and the
third for the last six years for which we have full data, 2016e2021.
Information on gender and country affiliation is only captured for
first authors; we believe this is a fair reflection of intellectual
ownership, probably more so than weighing all authors equally in
summary statistics. We recognize that characterizing the binary
gender of individuals is problematic, and a crude measure of gender
diversity. We also note that country of affiliation is not a proxy for
‘race,’ but rather pinpoints other characteristics related to power
dynamics, e.g., where the training, funding, and intellectual
ownership resides.
In the earliest years (1972e1977), the majority of papers were
single-authored (63%) and first-authored by men (87%). Only 12%
had 3 or more authors, with the most-authored paper being a
single one with 6 authors. Comparable demographics held from
1986 to 1991, with a majority single authorship (52%) and male first
authorship (82%), though the percentages did decrease in both
cases. In contrast, for the most recent years, only 6% of papers are
single-authored and 80% have 3 or more authors, while male first
authorship has dropped to 59%. This shifting dynamic points to a
discipline whose outputs are produced by larger, collaborative, and
more diverse teams.
However, although there have been substantial demographic
changes in terms of gender parity and author number since JHE was
established, there has been almost no change in terms of country of
origin of the first author. In the initial founding years from 1972 to
1977, 90% of papers were from Western countries, while less than
3% were from Africa and South America, numbers that shifted little
after editorial oversight began to include the USA (1986e1991).
Comparing this to today, there has been virtually no change in first-
authorship from Africa and South America over the last 50 years.
Moreover, in 2016e2021, only 3 of these papers come from South
America, while of the remaining 25 with first author affiliations in
Africa, all but 4 are from South Africa. Turning to Asia, while there
has been an almost 5% increase in first authors from Australasia
from the earliest years to today, from 2016 to 2021, there is only a
single paper where the first author has their primary affiliation in
South Asia, and no first authors have their primary affiliation in
Southeast Asia. Given the journal thrust, a low number of first
authors from South America, where there is not a deep fossil record
of human evolution, might be expected, but similar expectations do
not hold for Africa, South or Southeast Asia, nordgiven this argu-
mentdshould we have very high numbers from other countries
without relevant ancient material, such as North America.
We believe that, in the next 50 years, JHE should focus on using
the journal's power as gatekeepers of a collective norm for the
discipline (sensu Anto  n, 2022) to diversify who holds the status,
power, and authority, and therefore controls the process and
narrative, in order to be a transformative player in the growth of a Figure 5. Demographics of authorship in Journal of Human Evolution: 1972e1977 (A),
richer and more sustainable science. As has recently been pointed 1986e1991 (B), and 2016e2021 (C). Infographics created in Visme (Easy WebContent,
Inc., Rockville).

7 out (Anto n, 2022; Taylor and Zanolli, 2022), JHE has made great
For transparency, one of us (R.R.A.) had a long-term editorial role (Associate
Editor or Book Review Editor) for JHE for more than a decade and a half strides in some respects (e.g., double-blind reviews, gender parity
(2004e2012 and 2014e2020), across the tenures of numerous Editors-in-Chief. in the Editorial Board), but global diversity of authorship is not one
15
L. Schroeder and R.R. Ackermann
of those. Anto n details many possible practices that could be
incorporated into changing the discipline to one that is more
diverse and inclusive, and we concur with their suggestions. We
wish to highlight Anto  n's point that ethically sound, inclusive
research needs to be a priority, and based on the data presented
here but also our own experiences as scholars from or residing in
the Global South, helicopter research particularly in Africa (e.g.,
Nature Editorial, 2022) is a key concern. We believe that one
possible reason for such practice is a reliance on academic
networks established in formative years as graduate students and
early career scientists, and the difficulty of establishing comparable
relationships across continents and cultures, as well as mandates to
train students from your own institution. Given these issues, we
suggest that a key intervention that JHE could make would be to
actively seek out editorial board membership (including EICs and
AEs) from diverse backgrounds and geographies, which will begin
the process of breaking down siloed networks, especially as they
will provide different perspectives and recommend different po-
tential reviewers (we note that the current co-EICs have pledged
their commitment to diversity and inclusion in all aspects of the
journal, and we thus anticipate positive change in the near future8).
In conjunction, JHE could implement a system for identifying and
recruiting reviewers from outside of North America and Europe.
Journal of Human Evolution could also work to incentivize re-
searchers from the Global North to engage meaningfully with
students, researchers, and communities in the countries whose
heritage is being studied, including by encouraging more generous
authorship practices (as discussed in Anto  n, 2022), but also by
encouraging practices that include authors from diverse countries
earlier in the stage of research design (such as by explicitly
requesting this information at submission, and therefore normal-
izing it).
Clearly although the journaldand our disciplinedhas made
good strides in terms of the representativity and power of women,
in concert with shifting cultural norms and the maturation of our
discipline and society, there is a considerable way to go to capitalize
on the diversity of human knowledge from a more globally repre-
sentative authorship. Because diverse teams are known to result in
better science (Hong and Page, 2004; Apfelbaum et al., 2014;
Freeman and Huang, 2014; Aminpour et al., 2021), this needs to be a
priority for the journal and the discipline going forward. Although
we cannot change the past, researchers could also make a more
concerted effort to seek out and highlight diverse voices who did
contribute historically but who have largely disappeared in narra-
tives of our origins, as we tried to do here with the work of Roberta
Hall, as well as the voices who are not well-represented in the
literature despite their contributions. In conclusion, and in the
spirit and context of our call to move beyond the adaptationist
paradigm in human evolution, a change in the demographics of the
producers of our narratives is key for new paradigms to be formed
and actualized.
Declaration of competing interest
The authors have no conflicts of interest to declare.
Acknowledgments
We thank the funding agencies that have supported our
research on these topics over the past two decades: Palae-
ontological Scientific Trust (L.S.), The Leakey Foundation (L.S.,
8
https://www.sciencedirect.com/journal/journal-of-human-evolution/about/
announcements#diversity-inclusion-pledge-journal-of-human-evolution.
16
Journal of Human Evolution 174 (2023) 103296
R.R.A.) the South African National Research Foundation (L.S., R.R.A.),
the DST/NRF Centre of Excellence in Palaeosciences (COE-Pal;
R.R.A.), the National Science Foundation (R.R.A.), the Natural Sci-
ences and Engineering Research Council of Canada (Discovery
Grant RGPIN-2020-04159 to L.S.), and the Connaught Fund of the
University of Toronto (New Researcher Award to L.S.). We are
grateful to the many institutions and individuals for access to
comparative fossil and extant mammal, primate, and human
materials in their care: E. Mbua, P. Kiura, and the National Museums
of Kenya; the National Museum and House of Culture of Tanzania;
National Museum of Ethiopia; S. Potze and the Ditsong Museum; B.
Billings and the School of Anatomical Sciences of the University of
the Witwatersrand; B. Zipfel and the Evolutionary Studies Institute
at the University of the Witwatersrand; W. Seconna and the Iziko
South African Museum; Y. Haile-Selassie, L.M. Jellema and the
Cleveland Museum of Natural History; F. Schrenk, O. Kullmer, and C.
Hemm and the Senckenberg Forschungsinstitut; Burton Lim and
the Royal Ontario Museum, Robert Feranec and Joseph Bopp and
the New York State Museum, and Darrin Lunde and John Ososky
and the Smithsonian National Museum of Natural History. For ac-
cess to the canid data, we thank to N. Zdjelar. Finally, we would like
to thank A.B. Taylor and C. Zanolli for inviting us to contribute this
piece to ‘The 50th Anniversary of Journal of Human Evolution:
Current and Future Directions in Reconstructing our Past’ Virtual
Special Issue, as well as L. Hlusko and two anonymous reviewers for
their thoughtful comments on a previous version of our
manuscript.
Supplementary Online Material
Supplementary Online Material related to this article can be
found at https://doi.org/10.1016/j.jhevol.2022.103296.
References
Abbott, R., Albach, D., Ansell, S., Arntzen, J.W., Baird, S.J.E., Bierne, N., Boughman, J.,
Brelsford, A., Buerkle, C.A., Buggs, R., Butlin, R.K., Dieckmann, U.,
Eroukhmanoff, F., Grill, A., Cahan, S.H., Hermansen, J.S., Hewitt, G., Hudson, A.G.,
Jiggins, C., Jones, J., Keller, B., Marczewski, T., Mallet, J., Martinez-Rodriguez, P.,
Mo €st, M., Mullen, S., Nichols, R., Nolte, A.W., Parisod, C., Pfennig, K., Rice, A.M.,
€ino
€ l€
Ritchie, M.G., Seifert, B., Smadja, C.M., Stelkens, R., Szymura, J.M., Va a, R.,
Wolf, J.B.W., Zinner, D., 2013. Hybridization and speciation. J. Evol. Biol. 26,
229e246.
Abi-Rached, L., Jobin, M.J., Kulkarni, S., McWhinnie, A., Dalva, K., Gragert, L.,
Babrzadeh, F., Gharizadeh, B., Luo, M., Plummer, F.A., Kimani, J., 2011. The
shaping of modern human immune systems by multiregional admixture with
archaic humans. Science 334, 89e94.
Ackermann, R.R., 2010. Phenotypic traits of primate hybrids: Recognizing admixture
in the fossil record. Evol. Anthropol. 19, 258e270.
Ackermann, R.R., Arnold, M.L., Baiz, M.D., Cahill, J.A., Corte s-Ortiz, L., Evans, B.J.,
Grant, B.R., Grant, P.R., Hallgrimsson, B., Humphreys, R.A., 2019. Hybridization in
human evolution: Insights from other organisms. Evol. Anthropol. 28, 189e209.
Ackermann, R.R., Bishop, J.M., 2010. Morphological and molecular evidence reveals
recent hybridization between gorilla taxa. Evolution 64, 271e290.
Ackermann, R.R., Brink, J.S., Vrahimis, S., De, K.B., 2010. Hybrid wildebeest (Artio-
dactyla: Bovidae) provide further evidence for shared signatures of admixture
in mammalian crania. South Afr. J. Sci. 106, 1e5.
Ackermann, R.R., Cheverud, J.M., 2002. Discerning evolutionary processes in pat-
terns of tamarin (genus Saguinus) craniofacial variation. Am. J. Phys. Anthropol.
117, 260e271.
Ackermann, R.R., Cheverud, J.M., 2004. Detecting genetic drift versus selection in
human evolution. Proc. Natl. Acad. Sci. USA 101, 17946e17951.
Ackermann, R.R., Mackay, A., Arnold, M.L., 2016. The hybrid origin of “modern”
humans. Evol. Biol. 43, 1e11.
Ackermann, R.R., Rogers, J., Cheverud, J.M., 2006. Identifying the morphological
signatures of hybridization in primate and human evolution. J. Hum. Evol. 51,
632e645.
Ackermann, R.R., Schroeder, L., Rogers, J., Cheverud, J.M., 2014. Further evidence for
phenotypic signatures of hybridization in descendant baboon populations.
J. Hum. Evol. 76, 54e62.
Adavoudi, R., Pilot, M., 2022. Consequences of hybridization in mammals: A sys-
tematic review. Genes 13, 50.
L. Schroeder and R.R. Ackermann
Aminpour, P., Gray, S.A., Singer, A., Scyphers, S.B., Jetter, A.J., Jordan, R., Murphy, R.,
Grabowski, J.H., 2021. The diversity bonus in pooling local knowledge about
complex problems. Proc. Natl. Acad. Sci. USA 118, e2016887118.
Anderson, E., 1953. Introgressive hybridization. Biol. Rev. 28, 280e307.
Anderson, W., 2012. Racial hybridity, physical anthropology, and human biology
in the colonial laboratories of the United States. Curr. Anthropol. 53,
S95eS107.
Anton, S.C., 2022. JHE 50th anniversary: What does a journal owe its discipline?
J. Hum. Evol. 169, 103232.
Apfelbaum, E.P., Phillips, K.W., Richeson, J.A., 2014. Rethinking the baseline in di-
versity research: Should we be explaining the effects of homogeneity? Perspect.
Psychol. Sci. 9, 235e244.
Aponte, J.D., Katz, D.C., Roth, D.M., Vidal-García, M., Liu, W., Andrade, F.,
Roseman, C.C., Murray, S.A., Cheverud, J., Graf, D., 2021. Relating multivariate
shapes to genescapes using phenotype-biological process associations for
craniofacial shape. eLife 10, e68623.
Aristide, L., Rosenberger, A.L., Tejedor, M.F., Perez, S.I., 2015. Modeling lineage and
phenotypic diversification in the New World monkey (Platyrrhini, Primates)
radiation. Mol. Phylogenet. Evol. 82, 375e385.
Arnold, M.L., 2015. Divergence with Genetic Exchange. Oxford University Press,
Oxford.
Assis, A.P.A., Rossoni, D.M., Patton, J.L., Marroig, G., 2017. Evolutionary processes and
its environmental correlates in the cranial morphology of western chipmunks
(Tamias). Evolution 71, 595e609.
Athreya, S., Ackermann, R.R., 2020. Colonialism and narratives of human origins in
Asia and Africa. In: Porr, M., Matthews, J. (Eds.), Interrogating Human Origins.
Routledge, London, pp. 72e95.
Athreya, S., Hopkins, A., 2021. Conceptual issues in hominin taxonomy: Homo hei-
delbergensis and an ethnobiological reframing of species. Am. J. Phys. Anthropol.
175, 4e26.
Baab, K.L., 2018. Evolvability and craniofacial diversification in genus Homo. Evo-
lution 72, 2781e2791.
Baab, K.L., 2021. Reconstructing cranial evolution in an extinct hominin. Proc. R. Soc.
B 288, 20202604.
Barton, N.H., 2001. Speciation. Trends Ecol. Evol. 16, 325.
Barton, N.H., 2013. Does hybridisation influence speciation? J. Evol. Biol. 26,
267e269.
~o, J., 2010. Dental
Bayle, P., Macchiarelli, R., Trinkaus, E., Duarte, C., Mazurier, A., Zilha
maturational sequence and dental tissue proportions in the early Upper
Paleolithic child from Abrigo do Lagar Velho, Portugal. Proc. Natl. Acad. Sci. USA
107, 1338e1342.
Berner, D., Salzburger, W., 2015. The genomics of organismal diversification illu-
minated by adaptive radiations. Trends Genet. 31, 491e499.
Bernstein, I.S., 1974. Birth of two second generation hybrid macaques. J. Hum. Evol.
3, 205e206.
Betti, L., Balloux, F., Amos, W., Hanihara, T., Manica, A., 2009. Distance from Africa,
not climate, explains within-population phenotypic diversity in humans. Proc.
R. Soc. B 276, 809e814.
Betti, L., Balloux, F., Hanihara, T., Manica, A., 2010. The relative role of
drift and selection in shaping the human skull. Am. J. Phys. Anthropol. 141,
76e82.
Betti, L., Manica, A., 2018. Human variation in the shape of the birth canal is sig-
nificant and geographically structured. Proc. R. Soc. B 285, 20181807.
Betti, L., von Cramon-Taubadel, N., Manica, A., Lycett, S.J., 2014. The interaction of
neutral evolutionary processes with climatically-driven adaptive changes in the
3D shape of the human os coxae. J. Hum. Evol. 73, 64e74.
Bilsborough, A., 1973. A multivariate study of evolutionary change in the hominid
cranial vault and some evolution rates. J. Hum. Evol. 2, 387e403.
Bilsborough, A., 1976. Patterns of evolution in Middle Pleistocene hominids. J. Hum.
Evol. 5, 423e439.
Boyer, S.H., Noyes, A.N., Timmons, C.F., Young, R.A., 1972. Primate hemoglobins:
Polymorphisms and evolutionary patterns. J. Hum. Evol. 1, 515e543.
Boyle, E.A., Li, Y.I., Pritchard, J.K., 2017. An expanded view of complex traits: From
polygenic to omnigenic. Cell 169, 1177e1186.
Brand, C.M., Colbran, L.L., Capra, J.A., 2022. Predicting archaic hominin phenotypes
from genomic data. Annu. Rev. Genomics Hum. Genet. 23, 591e612.
Brasil, M.F., Monson, T.A., Schmitt, C.A., Hlusko, L.J., 2020. A genotype:phenotype
approach to testing taxonomic hypotheses in hominids. Sci. Nat. 107, 40.
€uer, G., 1984. The “Afro-European sapiens-hypothesis” and hominid evolution in
Bra
East Asia during the late Middle and Upper Pleistocene. Cour. Forsch. Inst.
Senckenberg 69, 145e165.
€uer, G., Leakey, R.E., 1986. The ES-11693 cranium from Eliye Springs, West Tur-
Bra
kana, Kenya. J. Hum. Evol. 15, 289e312.
Buck, L.T., Katz, D.C., Ackermann, R.R., Hlusko, L.J., Kanthaswamy, S., Weaver, T.D.,
2021. Effects of hybridization on pelvic morphology: A macaque model. J. Hum.
Evol. 159, 103049.
Carmon, J.L., 1963. Heterosis, combining ability, and maternal effects in mice.
J. Genet. 58, 225e231.
Carson, E.A., 2006. Maximum likelihood estimation of human craniometric heri-
tabilities. Am. J. Phys. Anthropol. 131, 169e180.
Caspari, R., 2018. Race, then and now: 1918 revisited. Am. J. Phys. Anthropol. 165,
924e938.
Chalifoux, L.V., Elliott, M.W., 1986. Congenital anomalies in two neonatal
tamarins (Saguinus oedipus and Saguinus fuscicollis). J. Med. Primatol. 15,
329e337.
17
Journal of Human Evolution 174 (2023) 103296
Charpentier, M.J., Widdig, A., Alberts, S.C., 2007. Inbreeding depression in non-
human primates: A historical review of methods used and empirical data.
Am. J. Primatol. 69, 1370e1386.
Chen, L., Wolf, A.B., Fu, W., Li, L., Akey, J.M., 2020. Identifying and interpreting
apparent Neanderthal ancestry in African individuals. Cell 180, 677e687.
Cheverud, J.M., 1988. A comparison of genetic and phenotypic correlations. Evolu-
tion 42, 958e968.
Dannemann, M., Andre s, A.M., Kelso, J., 2016. Introgression of Neandertal- and
Denisovan-like haplotypes contributes to adaptive variation in human toll-like
receptors. Am. J. Hum. Genet. 98, 22e33.
Dannemann, M., Kelso, J., 2017. The contribution of Neanderthals to phenotypic
variation in modern humans. Am. J. Hum. Genet. 101, 578e589.
Dannemann, M., Racimo, F., 2018. Something old, something borrowed: Admixture
and adaptation in human evolution. Curr. Opin. Genet. Dev. 53, 1e8.
Darwin, C., 1859. On the Origin of Species by Means of Natural Selection. Murray,
London.
Dasmahapatra, K.K., Walters, J.R., Briscoe, A.D., Davey, J.W., Whibley, A., Nadeau, N.J.,
Zimin, A.V., Hughes, D.S.T., Ferguson, L.C., Martin, S.H., Salazar, C., Lewis, J.J.,
Adler, S., Ahn, S.-J., Baker, D.A., Baxter, S.W., Chamberlain, N.L., Chauhan, R.,
Counterman, B.A., Dalmay, T., Gilbert, L.E., Gordon, K., Heckel, D.G., Hines, H.M.,
Hoff, K.J., Holland, P.W.H., Jacquin-Joly, E., Jiggins, F.M., Jones, R.T., Kapan, D.D.,
Kersey, P., Lamas, G., Lawson, D., Mapleson, D., Maroja, L.S., Martin, A., Moxon, S.,
Palmer, W.J., Papa, R., Papanicolaou, A., Pauchet, Y., Ray, D.A., Rosser, N.,
Salzberg, S.L., Supple, M.A., Surridge, A., Tenger-Trolander, A., Vogel, H.,
Wilkinson, P.A., Wilson, D., Yorke, J.A., Yuan, F., Balmuth, A.L., Eland, C.,
Gharbi, K., Thomson, M., Gibbs, R.A., Han, Y., Jayaseelan, J.C., Kovar, C.,
Mathew, T., Muzny, D.M., Ongeri, F., Pu, L.-L., Qu, J., Thornton, R.L., Worley, K.C.,
Wu, Y.-Q., Linares, M., Blaxter, M.L., ffrench-Constant, R.H., Joron, M.,
Kronforst, M.R., Mullen, S.P., Reed, R.D., Scherer, S.E., Richards, S., Mallet, J.,
Owen McMillan, W., Jiggins, C.D., The Heliconius Genome Consortium, 2012.
Butterfly genome reveals promiscuous exchange of mimicry adaptations among
species. Nature 487, 94e98.
de Oliveira, F.B., Porto, A., Marroig, G., 2009. Covariance structure in the skull of
Catarrhini: A case of pattern stasis and magnitude evolution. J. Hum. Evol. 56,
417e430.
Delson, E., Eldredge, N., Tattersall, I., 1977. Reconstruction of hominid phylogeny: A
testable framework based on cladistic analysis. J. Hum. Evol. 6, 263e278.
Detwiler, K.M., 2019. Mitochondrial DNA analyses of Cercopithecus monkeys reveal a
localized hybrid origin for C. mitis doggetti in Gombe National Park, Tanzania.
Int. J. Primatol. 40, 28e52.
Diniz-Filho, J.A.F., Raia, P., 2017. Island Rule, quantitative genetics and brainebody
size evolution in Homo floresiensis. Proc. R. Soc. B 284, 20171065.
Dobzhansky, T., 1937. Genetics and the Origin of Species. Columbia Univ. Press, New
York.
Dowell, R.D., Ryan, O., Jansen, A., Cheung, D., Agarwala, S., Danford, T.,
Bernstein, D.A., Rolfe, P.A., Heisler, L.E., Chin, B., Nislow, C., Giaever, G.,
Phillips, P.C., Fink, G.R., Gifford, D.K., Boone, C., 2010. Genotype to phenotype: A
complex problem. Science 328, 469.
~o, J.,
Duarte, C., Maurício, J., Pettitt, P.B., Souto, P., Trinkaus, E., van der Plicht, H., Zilha
1999. The early Upper Paleolithic human skeleton from the Abrigo do Lagar
Velho (Portugal) and modern human emergence in Iberia. Proc. Natl. Acad. Sci.
USA 96, 7604e7609.
Dunbar, R.I.M., Dunbar, P., 1974. On hybridization between Theropithecus gelada and
Papio anubis in the wild. J. Hum. Evol. 3, 187e192.
Durvasula, A., Sankararaman, S., 2020. Recovering signals of ghost archaic intro-
gression in African populations. Sci. Adv. 6, eaax5097.
Eichel, K.A., Ackermann, R.R., 2016. Variation in the nasal cavity of baboon hybrids
with implications for late Pleistocene hominins. J. Hum. Evol. 94, 134e145.
Falconer, D.S., 1960. Introduction to Quantitative Genetics. Oliver and Boyd, Edin-
burgh/London.
Falconer, D.S., Mackay, F.C., 1996. Introduction to Quantitative Genetics, Ed. 4.
Longmans Green, Harlow.
Fisher, R., 1918. The correlation between relatives on supposition of Mendel in-
heritance. Trans. R. Soc. Edinburgh 52, 399e433.
Fisher, R.A., 1930. The Genetical Theory of Natural Selection. Clarendon Press,
Oxford.
Freeman, R.B., Huang, W., 2014. Collaboration: Strength in diversity. Nature 513,
305.
Fu, Q., Hajdinjak, M., Moldovan, O.T., Constantin, S., Mallick, S., Skoglund, P.,
Patterson, N., Rohland, N., Lazaridis, I., Nickel, B., Viola, B., Prüfer, K., Meyer, M.,
€€
Kelso, J., Reich, D., Pa abo, S., 2015. An early modern human from Romania with a
recent Neanderthal ancestor. Nature 524, 216e219.
Fu, Q., Li, H., Moorjani, P., Jay, F., Slepchenko, S.M., Bondarev, A.A., Johnson, P.L.F.,
Aximu-Petri, A., Prüfer, K., de Filippo, C., Meyer, M., Zwyns, N., Salazar-
García, D.C., Kuzmin, Y.V., Keates, S.G., Kosintsev, P.A., Razhev, D.I.,
Richards, M.P., Peristov, N.V., Lachmann, M., Douka, K., Higham, T.F.G.,
Slatkin, M., Hublin, J.-J., Reich, D., Kelso, J., Viola, T.B., Pa€€
abo, S., 2014. Genome
sequence of a 45,000-year-old modern human from western Siberia. Nature
514, 445e449.
Gabow, S.L., 1977. Population structure and the rate of hominid brain evolution.
J. Hum. Evol. 6, 643e665.
Galloway, J., Cresko, W.A., Ralph, P., 2020. A few stickleback suffice for the transport
of alleles to new lakes. G3 Genes|Genomes|Genetics 10, 505e514.
Gijzen, A., 1973. Two accidentally bred monkey-hybrids grew up. J. Hum. Evol. 2,
27e29.
L. Schroeder and R.R. Ackermann
Gillespie, R.G., Bennett, G.M., De Meester, L., Feder, J.L., Fleischer, R.C., Harmon, L.J.,
Hendry, A.P., Knope, M.L., Mallet, J., Martin, C., Parent, C.E., Patton, A.H.,
Pfennig, K.S., Rubinoff, D., Schluter, D., Seehausen, O., Shaw, K.L., Stacy, E.,
Stervander, M., Stroud, J.T., Wagner, C., Wogan, G.O.U., 2020. Comparing adap-
tive radiations across space, time, and taxa. J. Hered. 111, 1e20.
Gokcumen, O., 2020. Archaic hominin introgression into modern human genomes.
Am. J. Phys. Anthropol. 171, 60e73.
mez-Robles, A., Smaers, J.B., Holloway, R.L., Polly, P.D., Wood, B.A., 2017. Brain
Go
enlargement and dental reduction were not linked in hominin evolution. Proc.
Natl. Acad. Sci. USA 114, 468e473.
Goodwin, H.T., 1998. Supernumerary teeth in Pleistocene, recent, and hybrid in-
dividuals of the Spermophilus richardsonii complex (Sciuridae). J. Mammal. 79,
1161e1169.
Gould, S.J., Lewontin, R., 1979. The spandrels of San Marco and the Panglossian
paradigm: A critique of the adaptationist programme. Proc. R. Soc. B 205,
581e598.
Grabowski, M., 2016. Bigger brains led to bigger bodies?: The correlated evolution
of human brain and body size. Curr. Anthropol. 57, 174e196.
Grabowski, M., Roseman, C.C., 2015. Complex and changing patterns of nat-
ural selection explain the evolution of the human hip. J. Hum. Evol. 85,
94e110.
Grant, P.R., Grant, B.R., Markert, J.A., Keller, L.F., Petren, K., 2004. Convergent evo-
lution of Darwin's finches caused by introgressive hybridization and selection.
Evolution 58, 1588e1599.
Grant, V., 1981. Plant Speciation. Columbia University Press, New York.
Green, R.E., Krause, J., Briggs, A.W., Maricic, T., Stenzel, U., Kircher, M., Patterson, N.,
Li, H., Zhai, W., Fritz, M.H.-Y., Hansen, N.F., Durand, E.Y., Malaspinas, A.-S.,
Jensen, J.D., Marques-Bonet, T., Alkan, C., Prüfer, K., Meyer, M., Burbano, H.A.,
Good, J.M., Schultz, R., Aximu-Petri, A., Butthof, A., Ho € ber, B., Ho €ffner, B.,
Siegemund, M., Weihmann, A., Nusbaum, C., Lander, E.S., Russ, C., Novod, N.,
Affourtit, J., Egholm, M., Verna, C., Rudan, P., Brajkovic, D., Kucan, Z.,  Gusic, I.,
Doronichev, V.B., Golovanova, L.V., Lalueza-Fox, C., de la Rasilla, M., Fortea, J.,
Rosas, A., Schmitz, R.W., Johnson, P.L.F., Eichler, E.E., Falush, D., Birney, E.,
Mullikin, J.C., Slatkin, M., Nielsen, R., Kelso, J., Lachmann, M., Reich, D., P€ €bo, S.,
aa
2010. A draft sequence of the Neandertal genome. Science 328, 710e722.
Gregory, M.D., Kippenhan, J.S., Eisenberg, D.P., Kohn, P.D., Dickinson, D., Mattay, V.S.,
Chen, Q., Weinberger, D.R., Saad, Z.S., Berman, K.F., 2017. Neanderthal-derived
genetic variation shapes modern human cranium and brain. Sci. Rep. 7, 6308.
Grieco, T.M., Rizk, O.T., Hlusko, L.J., 2013. A modular framework characterizes micro-
and macroevolution of Old World monkey dentitions. Evolution 67, 241e259.
Gunz, P., Tilot, A.K., Wittfeld, K., Teumer, A., Shapland, C.Y., van Erp, T.G.M.,
Dannemann, M., Vernot, B., Neubauer, S., Guadalupe, T., Ferna ndez, G.,
Brunner, H.G., Enard, W., Fallon, J., Hosten, N., Vo €lker, U., Profico, A., Di
Vincenzo, F., Manzi, G., Kelso, J., St. Pourcain, B., Hublin, J.-J., Franke, B., P€
aa€bo, S.,
Macciardi, F., Grabe, H.J., Fisher, S.E., 2019. Neandertal introgression sheds light
on modern human endocranial globularity. Curr. Biol. 29, 120e127 e5.
Hackinger, S., Kraaijenbrink, T., Xue, Y., Mezzavilla, M., van Driem, G., Jobling, M.A.,
de Knijff, P., Tyler-Smith, C., Ayub, Q., 2016. Wide distribution and altitude
correlation of an archaic high-altitude-adaptive EPAS1 haplotype in the
Himalayas. Hum. Genet. 135, 393e402.
Hajdinjak, M., Mafessoni, F., Skov, L., Vernot, B., Hübner, A., Fu, Q., Essel, E., Nagel, S.,
Nickel, B., Richter, J., Moldovan, O.T., Constantin, S., Endarova, E., Zahariev, N.,
Spasov, R., Welker, F., Smith, G.M., Sinet-Mathiot, V., Paskulin, L., Fewlass, H.,
Talamo, S., Rezek, Z., Sirakova, S., Sirakov, N., McPherron, S.P., Tsanova, T.,
Hublin, J.-J., Peter, B.M., Meyer, M., Skoglund, P., Kelso, J., Pa €a
€bo, S., 2021. Initial
Upper Palaeolithic humans in Europe had recent Neanderthal ancestry. Nature
592, 253e257.
Haldane, J.B.S., 1957. The cost of natural selection. J. Genet. 55, 511.
Hall, R., 1977. Paleobiology and systematics of canids and hominids. J. Hum. Evol. 6,
519e531.
Hall, R.L., 1978. Variability and speciation in canids and hominids. In:
Hall, R.L., Sharp, H.S. (Eds.), Wolf and Man. Academic Press, New York,
pp. 153e177.
Hammer, Ø., Harper, D.A.T., Ryan, P.D., 2001. PAST: Paleontological statistics soft-
ware package for education and data analysis. Palaeontol. Electron. 4, 9.
Hammer, M.F., Woerner, A.E., Mendez, F.L., Watkins, J.C., Wall, J.D., 2011. Genetic
evidence for archaic admixture in Africa. Proc. Natl. Acad. Sci. USA 108,
15123e15128.
Hanihara, T., 2008. Morphological variation of major human populations based on
nonmetric dental traits. Am. J. Phys. Anthropol. 136, 169e182.
Hanihara, T., Ishida, H., 2005. Metric dental variation of major human populations.
Am. J. Phys. Anthropol. 128, 287e298.
Hanihara, T., Ishida, H., Dodo, Y., 2003. Characterization of biological diversity
through analysis of discrete cranial traits. Am. J. Phys. Anthropol. 121, 241e251.
Hanot, P., Herrel, A., Guintard, C., Cornette, R., 2019. Unravelling the hybrid vigor in
domestic equids: The effect of hybridization on bone shape variation and
covariation. BMC Evol. Biol. 19, 188.
Hardin, A.M., 2020. Genetic correlations in the rhesus macaque dentition. J. Hum.
Evol. 148, 102873.
Harrison, T., 2016. The fossil record and evolutionary history of hylobatids. In:
Reichard, U.H., Hirai, H., Barelli, C. (Eds.), Evolution of Gibbons and Siamang:
Phylogeny, Morphology, and Cognition, Developments in Primatology: Progress
and Prospects. Springer, New York, pp. 91e110.
18
Journal of Human Evolution 174 (2023) 103296
Harvati, K., Ackermann, R.R., 2022. Merging morphological and genetic evidence to
assess hybridization in Western Eurasian late Pleistocene hominins. Nat. Ecol.
Evol. 6, 1573e1585.
Harvati, K., Gunz, P., Grigorescu, D., 2007. Cioclovina (Romania): Affinities of an
early modern European. J. Hum. Evol. 53, 732e746.
Harvati, K., Weaver, T.D., 2006. Human cranial anatomy and the differential pres-
ervation of population history and climate signatures. Anat. Rec. 288,
1225e1233.
Heide-Jørgensen, M.P., Reeves, R.R., 1993. Description of an anomalous monodontid
skull from west Greenland: A possible hybrid? Mar. Mamm. Sci. 9, 258e268.
Henn, B.M., Cavalli-Sforza, L.L., Feldman, M.W., 2012. The great human expansion.
Proc. Natl. Acad. Sci. USA 109, 17758e17764.
Hlazo, N., 2018. Variation and the evolutionary drivers of diversity in the genus
Paranthropus. M.Sc. Thesis. University of Cape Town.
Hlazo, N., Ritzman, T.R., Schroeder, L., Ackermann, R.R., 2018. The role of selection in
shaping the cranio-mandibular morphology of Paranthropus. Am. J. Phys.
Anthropol. 165, 121.
Hlusko, L.J., 2004. Integrating the genotype and phenotype in hominid paleon-
tology. Proc. Natl. Acad. Sci. USA 101, 2653e2657.
Hlusko, L.J., 2016. Elucidating the evolution of hominid dentition in the age of
phenomics, modularity, and quantitative genetics. Ann. Anat. 203, 3e11.
Hlusko, L.J., Lease, L.R., Mahaney, M.C., 2006. Evolution of genetically correlated
traits: Tooth size and body size in baboons. Am. J. Phys. Anthropol. 131,
420e427.
Hlusko, L.J., Sage, R.D., Mahaney, M.C., 2011. Modularity in the mammalian denti-
tion: Mice and monkeys share a common dental genetic architecture. J. Exp.
Zool. B Mol. Dev. Evol. 316, 21e49.
Hlusko, L.J., Schmitt, C.A., Monson, T.A., Brasil, M.F., Mahaney, M.C., 2016. The
integration of quantitative genetics, paleontology, and neontology reveals ge-
netic underpinnings of primate dental evolution. Proc. Natl. Acad. Sci. USA 113,
9262e9267.
Hlusko, L.J., Suwa, G., Kono, R.T., Mahaney, M.C., 2004. Genetics and the evolution of
primate enamel thickness: A baboon model. Am. J. Phys. Anthropol. 124,
223e233.
Hong, L., Page, S.E., 2004. Groups of diverse problem solvers can outperform
groups of high-ability problem solvers. Proc. Natl. Acad. Sci. USA 101,
16385e16389.
Houle, D., Govindaraju, D.R., Omholt, S., 2010. Phenomics: The next challenge. Nat.
Rev. Genet. 11, 855e866.
Hoyer, B.H., van de Velde, N.W., Goodman, M., Roberts, R.B., 1972. Examination of
hominid evolution by DNA sequence homology. J. Hum. Evol. 1, 645e649.
Hu, Y., Ding, Q., He, Y., Xu, S., Jin, L., 2015. Reintroduction of a homocysteine level-
associated allele into East Asians by Neanderthal introgression. Mol. Biol. Evol.
32, 3108e3113.
Huerta-Sa nchez, E., Jin, X., Asan, Bianba, Z., Peter, B.M., Vinckenbosch, N., Liang, Y.,
Yi, X., He, M., Somel, M., Ni, P., Wang, B., Ou, X., Huasang, Luosang, J., Cuo, Z.X.P.,
Li, K., Gao, G., Yin, Y., Wang, W., Zhang, X., Xu, X., Yang, H., Li, Y., Wang, Jian,
Wang, Jun, Nielsen, R., 2014. Altitude adaptation in Tibetans caused by intro-
gression of Denisovan-like DNA. Nature 512, 194e197.
Huff, C.D., Xing, J., Rogers, A.R., Witherspoon, D., Jorde, L.B., 2010. Mobile elements
reveal small population size in the ancient ancestors of Homo sapiens. Proc.
Natl. Acad. Sci. USA 107, 2147e2152.
Huxley, J., 1942. Evolution, The Modern Synthesis. George Allen & Unwin, London.
Irish, J.D., Grabowski, M., 2021. Relative tooth size, Bayesian inference, and Homo
naledi. Am. J. Phys. Anthropol. 176, 262e282.
Irving-Pease, E.K., Muktupavela, R., Dannemann, M., Racimo, F., 2021. Quantitative
human paleogenetics: What can ancient DNA tell us about complex trait evo-
lution? Front. Genet. 12, 703541.
Isaac, G.L., 1975. Early hominids in action: A commentary on the contribution of
archeology to understanding the fossil record in East Africa. Yearb. Phys.
Anthropol. 19, 19e35.
International Commission on Zoological Nomenclature (ICZN), 1999. International
Code of Zoological Nomenclature. The International Trust for Zoological
Nomenclature, London. http://www.nhm.ac.uk/hosted-sites/iczn/code/.
Jacquard, A., 1977. Transmission of genes and transmission of characteristics. J. Hum.
Evol. 6, 733e734.
Jolly, C.J., 2001. A proper study for mankind: Analogies from the Papionin monkeys
and their implications for human evolution. Am. J. Phys. Anthropol. 116,
177e204.
Jolly, C.J., 2016. A life in evolutionary anthropology. Annu. Rev. Anthropol. 45, 1e15.
Juric, I., Aeschbacher, S., Coop, G., 2016. The strength of selection against Nean-
derthal introgression. PLoS Genet. 12, e1006340.
Kays, R., Curtis, A., Kirchman, J.J., 2010. Rapid adaptive evolution of northeastern
coyotes via hybridization with wolves. Biol. Lett. 6, 89e93.
Khrameeva, E.E., Bozek, K., He, L., Yan, Z., Jiang, X., Wei, Y., Tang, K., Gelfand, M.S.,
Prufer, K., Kelso, J., Paabo, S., Giavalisco, P., Lachmann, M., Khaitovich, P., 2014.
Neanderthal ancestry drives evolution of lipid catabolism in contemporary
Europeans. Nat. Commun. 5, 3584.
Kimbel, W.H., Delezene, L.K., 2009. “Lucy” redux: A review of research on Austral-
opithecus afarensis. Am. J. Phys. Anthropol. 140, 2e48.
Kimura, M., 1968. Evolutionary rate at the molecular level. Nature 217, 624e626.
Kimura, M., 1983. The Neutral Theory of Molecular Evolution. Cambridge University
Press, Cambridge.
L. Schroeder and R.R. Ackermann
Kimura, M., 1991. The neutral theory of molecular evolution: A review of recent
evidence. Jpn. J. Genet. 66, 367e386.
King, J.L., Jukes, T.H., 1969. Non-Darwinian evolution. Science 164, 788e798.
Kirkpatrick, M., Barrett, B., 2015. Chromosome inversions, adaptive cassettes and
the evolution of species' ranges. Mol. Ecol. 24, 2046e2055.
Kissel, M., Fuentes, A., 2021. The ripples of modernity: How we can extend paleo-
anthropology with the extended evolutionary synthesis. Evol. Anthropol. 30,
84e98.
Klein, R.G., 2003. Whither the Neanderthals? Science 299, 1525e1527.
Klein, R.G., 2009. The Human Career: Human Biological and Cultural Origins, third
ed. University of Chicago Press, Chicago.
Klingenberg, C.P., Leamy, L.J., Cheverud, J.M., 2004. Integration and modularity of
quantitative trait locus effects on geometric shape in the mouse mandible.
Genetics 166, 1909e1921.
Koertvelyessy, T., Thompson, A., 1975. A twins-method heritability estimate of
extremity surface temperatures during exposure to a standardized cold-stress.
J. Hum. Evol. 4, 235e249.
Kohn, L.A.P., Langton, L.B., Cheverud, J.M., 2001. Subspecific genetic differences in
the saddle-back tamarin (Saguinus fuscicollis) postcranial skeleton. Am. J. Pri-
matol. 54, 41e56.
Kohne, D.E., Chiscon, J.A., Hoyer, B.H., 1972. Evolution of primate DNA sequences.
J. Hum. Evol. 1, 627e644.
Koonin, E.V., 2016. Splendor and misery of adaptation, or the importance of neutral
null for understanding evolution. BMC Biol. 14, 114.
Kreitman, M., 1996. The neutral theory is dead. Long live the neutral theory. Bio-
essays 18, 678e683.
Kuhlwilm, M., Gronau, I., Hubisz, M.J., de Filippo, C., Prado-Martinez, J., Kircher, M.,
Fu, Q., Burbano, H.A., Lalueza-Fox, C., de la Rasilla, M., Rosas, A., Rudan, P.,
Brajkovic, D., Kucan, Z.,  Gusic, I., Marques-Bonet, T., Andre s, A.M., Viola, B.,
Pa€€
abo, S., Meyer, M., Siepel, A., Castellano, S., 2016. Ancient gene flow from early
modern humans into Eastern Neanderthals. Nature 530, 429e433.
Kurnianto, E., Shinjo, A., Suga, D., Uema, N., 1999. Diallel cross analysis of body
weight in subspecies of mice. Exp. Anim. 48, 277e283.
Lachance, J., Vernot, B., Elbers, C.C., Ferwerda, B., Froment, A., Bodo, J.-M., Lema, G.,
Fu, W., Nyambo, T.B., Rebbeck, T.R., Zhang, K., Akey, J.M., Tishkoff, S.A., 2012.
Evolutionary history and adaptation from high-coverage whole-genome se-
quences of diverse African hunter-gatherers. Cell 150, 457e469.
Lalueza-Fox, C., Ro €mpler, H., Caramelli, D., St€ aubert, C., Catalano, G., Hughes, D.,
Rohland, N., Pilli, E., Longo, L., Condemi, S., de la Rasilla, M., Fortea, J., Rosas, A.,
Stoneking, M., Scho €neberg, T., Bertranpetit, J., Hofreiter, M., 2007.
A melanocortin 1 receptor allele suggests varying pigmentation among Nean-
derthals. Science 318, 1453e1455.
Lande, R., 1976. Natural selection and random genetic drift in phenotypic evolution.
Evolution 30, 314e334.
Lande, R., 1979. Quantitative genetic analysis of multivariate evolution, applied to
brain: Body size allometry. Evolution 33, 402e416.
Lande, R., 2000. Quantitative genetics and phenotypic evolution. In: Singh, R.S.,
Krimbas, C.B. (Eds.), Evolutionary Genetics. From Molecules to Morphology.
Cambridge University Press, Cambridge, pp. 335e350.
Lande, R., Arnold, S.J., 1983. The measurement of selection on correlated characters.
Evolution 37, 1210e1226.
Langergraber, K.E., Prüfer, K., Rowney, C., Boesch, C., Crockford, C., Fawcett, K.,
Inoue, E., Inoue-Muruyama, M., Mitani, J.C., Muller, M.N., Robbins, M.M.,
Schubert, G., Stoinski, T.S., Viola, B., Watts, D., Wittig, R.M., Wrangham, R.W.,
Zuberbühler, K., Pa €€
abo, S., Vigilant, L., 2012. Generation times in wild chim-
panzees and gorillas suggest earlier divergence times in great ape and human
evolution. Proc. Natl. Acad. Sci. USA 109, 15716e15721.
Latham, A.G., Herries, A.I.R., 2004. The formation and sedimentary infilling of the
Cave of Hearths and Historic Cave complex, Makapansgat, South Africa. Geo-
archaeology 19, 323e342.
Lavelle, C.L.B., Moore, W.J., 1973. The incidence of agenesis and polygenesis in the
primate dentition. Am. J. Phys. Anthropol. 38, 671e679.
Leakey, R.E.F., Wood, B.A., 1973. New evidence of the genus Homo from East Rudolf,
Kenya. II. Am. J. Phys. Anthropol. 39, 355e368.
Leamy, L., 1982. Morphometric studies in inbred and hybrid house mice: I. Patterns
in the mean values. J. Hered. 73, 171e176.
Leamy, L., 1992. Morphometric studies in inbred and hybrid house mice. VII. Het-
erosis in fluctuating asymmetry at different ages. Acta Zool. Fennica 191,
111e119.
Lepre, C.J., Kent, D.V., 2015. Chronostratigraphy of KNM-ER 3733 and other Area 104
hominins from Koobi Fora. J. Hum. Evol. 86, 99e111.
Lerman, A., 1965. On rates of evolution of unit characters and character complexes.
Evolution 19, 16e25.
Lewontin, R.C., 1974. The Genetic Basis of Evolutionary Change. Columbia University
Press, New York.
Lewontin, R.C., Hubby, J.L., 1966. A molecular approach to the study of genic
heterozygosity in natural populations. II. Amount of variation and degree of
heterozygosity in natural populations of Drosophila pseudoobscura. Genetics 54,
595e609.
Lipson, M., Ribot, I., Mallick, S., Rohland, N., Olalde, I., Adamski, N.,
Broomandkhoshbacht, N., Lawson, A.M., Lo  pez, S., Oppenheimer, J.,
Stewardson, K., Asombang, R.N., Bocherens, H., Bradman, N., Culleton, B.J.,
Cornelissen, E., Crevecoeur, I., de Maret, P., Fomine, F.L.M., Lavachery, P.,
Mindzie, C.M., Orban, R., Sawchuk, E., Semal, P., Thomas, M.G., Van Neer, W.,
Veeramah, K.R., Kennett, D.J., Patterson, N., Hellenthal, G., Lalueza-Fox, C.,
19
Journal of Human Evolution 174 (2023) 103296
MacEachern, S., Prendergast, M.E., Reich, D., 2020. Ancient West African for-
agers in the context of African population history. Nature 577, 665e670.
Lofsvold, D., 1988. Quantitative genetics of morphological differentiation in Per-
omyscus. II. Analysis of selection and drift. Evolution 42, 54e67.
Lynch, M., Walsh, B., 1998. Genetics and Analysis of Quantitative Traits. Sinauer,
Sunderland, MA.
Machado, F.A., Marroig, G., Hubbe, A., 2022. The pre-eminent role of directional
selection in generating extreme morphological change in glyptodonts (Cingu-
lata; Xenarthra). Proc. R. Soc. B 289, 20212521.
Mackay, T.F.C., 2014. Epistasis and quantitative traits: Using model organisms to
study geneegene interactions. Nat. Rev. Genet. 15, 22e33.
Mallet, J., 2005. Hybridization as an invasion of the genome. Trends Ecol. Evol. 20,
229e237.
Mallet, J., 2007. Hybrid speciation. Nature 446, 279e283.
Mallet, J., Besansky, N., Hahn, M.W., 2016. How reticulated are species? Bioessays
38, 140e149.
Manica, A., Amos, W., Balloux, F., Hanihara, T., 2007. The effect of ancient population
bottlenecks on human phenotypic variation. Nature 448, 346e348.
Marks, J., 2007. Anthropological taxonomy as subject and object: The consequences
of descent from Darwin and Durkheim. Anthropol. Today 23, 7e12.
Marroig, G., Cheverud, J.M., 2004. Did natural selection or genetic drift
produce the cranial diversification of Neotropical monkeys? Am. Nat. 163,
417e428.
Marroig, G., Cheverud, J.M., 2005. Size as a line of least evolutionary resistance: Diet
and adaptive morphological radiation in New World monkeys. Evolution 59,
1128e1142.
Mathieson, I., 2021. The omnigenic model and polygenic prediction of complex
traits. Am. J. Hum. Genet. 108, 1558e1563.
Mathieson, I., Lazaridis, I., Rohland, N., Mallick, S., Patterson, N., Roodenberg, S.A.,
Harney, E., Stewardson, K., Fernandes, D., Novak, M., Sirak, K., Gamba, C.,
Jones, E.R., Llamas, B., Dryomov, S., Pickrell, J., Arsuaga, J.L., de Castro, J.M.B.,
Carbonell, E., Gerritsen, F., Khokhlov, A., Kuznetsov, P., Lozano, M., Meller, H.,
Mochalov, O., Moiseyev, V., Guerra, M.A.R., Roodenberg, J., Verge s, J.M.,
Krause, J., Cooper, A., Alt, K.W., Brown, D., Anthony, D., Lalueza-Fox, C., Haak, W.,
Pinhasi, R., Reich, D., 2015. Genome-wide patterns of selection in 230 ancient
Eurasians. Nature 528, 499e503.
Mayr, E., 1942. Systematics and the Origin of Species, from the Viewpoint of a
Zoologist. Columbia Univ. Press, New York.
McDougall, I., Brown, F.H., 2006. Precise 40Ar/39Ar geochronology for the upper
Koobi Fora Formation, Turkana Basin, northern Kenya. J. Geol. Soc. 163,
205e220.
McHenry, H.M., Brown, C.C., 2008. Side steps: The erratic pattern of hominin
postcranial change through time. J. Hum. Evol. 55, 639e651.
Melo, D., Garcia, G., Hubbe, A., Assis, A.P., Marroig, G., 2016. EvolQG - An R package
for evolutionary quantitative genetics. F1000Res. 4, 925.
Mendel, G., 1866. Versuche über pflanzen-hybriden. Verhandlungen des natur-
forschenden Vereines in Brünn 4, 3e47.
Meyer, M., Kircher, M., Gansauge, M.-T., Li, H., Racimo, F., Mallick, S., Schraiber, J.G.,
Jay, F., Prüfer, K., de Filippo, C., Sudmant, P.H., Alkan, C., Fu, Q., Do, R.,
Rohland, N., Tandon, A., Siebauer, M., Green, R.E., Bryc, K., Briggs, A.W.,
Stenzel, U., Dabney, J., Shendure, J., Kitzman, J., Hammer, M.F., Shunkov, M.V.,
Derevianko, A.P., Patterson, N., Andre s, A.M., Eichler, E.E., Slatkin, M., Reich, D.,
€€
Kelso, J., Pa abo, S., 2012. A high-coverage genome sequence from an archaic
Denisovan individual. Science 338, 222e226.
Milocco, L., Salazar-Ciudad, I., 2020. Is evolution predictable? Quantitative genetics
under complex genotype-phenotype maps. Evolution 74, 230e244.
Mishler, B.D., 1994. Cladistic analysis of molecular and morphological data. Am. J.
Phys. Anthropol. 94, 143e156.
Mozzi, A., Forni, D., Cagliani, R., Pozzoli, U., Clerici, M., Sironi, M., 2017. Distinct
selective forces and Neanderthal introgression shaped genetic diversity at
genes involved in neurodevelopmental disorders. Sci. Rep. 7, 6116.
Nagendran, L., Schroeder, L., 2022. Lessons from the coywolf (Canis latrans var.):
Patterns of mandibular integration in hybrid canids and its implications for the
hominin fossil record. Am. J. Biol. Anthropol. 177 (S73), 131.
Nakamichi, M., Nobuhara, H., Nobuhara, T., Nakahashi, M., Nigi, H., 1997. Birth rate
and mortality rate of infants with congenital malformations of the limbs in the
Awajishima free-ranging group of Japanese monkeys (Macaca fuscata). Am. J.
Primatol. 42, 225e234.
Nature Editorial, 2022. Nature addresses helicopter research and ethics dumping.
Nature 606, 7.
Norgard, E.A., Jarvis, J.P., Roseman, C.C., Maxwell, T.J., Kenney-Hunt, J.P.,
Samocha, K.E., Pletscher, L.S., Wang, B., Fawcett, G.L., Leatherwood, C.J.,
Wolf, J.B., Cheverud, J.M., 2009. Replication of long-bone length QTL in the F9-
F10 LG,SM advanced intercross. Mamm. Genome 20, 224e235.
Olson, E.C., Miller, R.L., 1999. Morphological Integration. University of Chicago Press,
Chicago.
Parsons, K.J., Son, Y.H., Craig Albertson, R., 2011. Hybridization promotes evolvability
in African cichlids: Connections between transgressive segregation and
phenotypic integration. Evol. Biol. 38, 306e315.
Petr, M., P€ €bo, S., Kelso, J., Vernot, B., 2019. Limits of long-term selection against
aa
Neandertal introgression. Proc. Natl. Acad. Sci. USA 116, 1639e1644.
Pilot, M., Moura, A.E., Okhlopkov, I.M., Mamaev, N.V., Manaseryan, N.H.,
Hayrapetyan, V., Kopaliani, N., Tsingarska, E., Alagaili, A.N.,
Mohammed, O.B., Ostrander, E.A., Bogdanowicz, W., 2021. Human-modified
canids in human-modified landscapes: The evolutionary consequences of
L. Schroeder and R.R. Ackermann
hybridization for grey wolves and free-ranging domestic dogs. Evol. Appl.
14, 2433e2456.
Ponce de Leo  n, M.S., Koesbardiati, T., Weissmann, J.D., Milella, M., Reyna-
Blanco, C.S., Suwa, G., Kondo, O., Malaspinas, A.-S., White, T.D., Zollikofer, C.P.E.,
2018. Human bony labyrinth is an indicator of population history and dispersal
from Africa. Proc. Natl. Acad. Sci. USA 115, 4128e4133.
Popadin, K., Gunbin, K., Peshkin, L., Annis, S., Fleischmann, Z., Franco, M.,
Kraytsberg, V., Markuzon, N., Ackermann, R.R., Khrapko, K., 2022. Mitochondrial
pseudogenes suggest repeated inter-species hybridization among direct human
ancestors. Genes 13, 810.
Posth, C., Wißing, C., Kitagawa, K., Pagani, L., van Holstein, L., Racimo, F.,
Wehrberger, K., Conard, N.J., Kind, C.J., Bocherens, H., Krause, J., 2017. Deeply
divergent archaic mitochondrial genome provides lower time boundary for
African gene flow into Neanderthals. Nat. Commun. 8, 16046.
Provine, W.B., 1971. The Origins of Theoretical Population Genetics. University of
Chicago Press, Chicago.
Prüfer, K., Posth, C., Yu, H., Stoessel, A., Spyrou, M.A., Deviese, T., Mattonai, M.,
Ribechini, E., Higham, T., Velemínský, P., Br u
zek, J., Krause, J., 2021. A genome
sequence from a modern human skull over 45,000 years old from Zlatý k  in
un
Czechia. Nat. Ecol. Evol. 5, 820e825.
Prüfer, K., Racimo, F., Patterson, N., Jay, F., Sankararaman, S., Sawyer, S., Heinze, A.,
Renaud, G., Sudmant, P.H., de Filippo, C., Li, H., Mallick, S., Dannemann, M.,
Fu, Q., Kircher, M., Kuhlwilm, M., Lachmann, M., Meyer, M., Ongyerth, M.,
Siebauer, M., Theunert, C., Tandon, A., Moorjani, P., Pickrell, J., Mullikin, J.C.,
Vohr, S.H., Green, R.E., Hellmann, I., Johnson, P.L.F., Blanche, H., Cann, H.,
Kitzman, J.O., Shendure, J., Eichler, E.E., Lein, E.S., Bakken, T.E., Golovanova, L.V.,
Doronichev, V.B., Shunkov, M.V., Derevianko, A.P., Viola, B., Slatkin, M., Reich, D.,
€a
Kelso, J., Pa €bo, S., 2014. The complete genome sequence of a Neanderthal from
the Altai Mountains. Nature 505, 43e49.
R Core Team, 2022. R: A language and environment for statistical computing. R
Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.
org/.
Racimo, F., Sankararaman, S., Nielsen, R., Huerta-Sa nchez, E., 2015. Evidence for
archaic adaptive introgression in humans. Nat. Rev. Genet. 16, 359e371.
Rathmann, H., Reyes-Centeno, H., 2020. Testing the utility of dental morphological
trait combinations for inferring human neutral genetic variation. Proc. Natl.
Acad. Sci. USA 117, 10769e10777.
Rajab, L.D., Hamdan, M.A.M., 2002. Supernumerary teeth: Review of the literature
and a survey of 152 cases. Int. J. Paediatr. Dent. 12, 244e254.
Rawlins, R.G., Kessler, M.J., 1983. Congenital and hereditary anomalies in the rhesus
monkeys (Macaca mulatta) of Cayo Santiago. Teratology 28, 169e174.
Reich, D., Green, R.E., Kircher, M., Krause, J., Patterson, N., Durand, E.Y., Viola, B.,
Briggs, A.W., Stenzel, U., Johnson, P.L.F., Maricic, T., Good, J.M., Marques-
Bonet, T., Alkan, C., Fu, Q., Mallick, S., Li, H., Meyer, M., Eichler, E.E.,
Stoneking, M., Richards, M., Talamo, S., Shunkov, M.V., Derevianko, A.P.,
€€
Hublin, J.-J., Kelso, J., Slatkin, M., Pa abo, S., 2010. Genetic history of an archaic
hominin group from Denisova Cave in Siberia. Nature 468, 1053e1060.
Reid, K., Bell, M.A., Veeramah, K.R., 2021. Threespine stickleback: A model system
for evolutionary genomics. Annu. Rev. Genom. Hum. Genet. 22, 357e383.
Relethford, J.H., 2004. Global patterns of isolation by distance based on genetic and
morphological data. Hum. Biol. 76, 499e513.
Relethford, J.H., Blangero, J., 1990. Detection of differential gene flow from patterns
of quantitative variation. Hum. Biol. 62, 5e25.
Reyes-Centeno, H., Rathmann, H., Hanihara, T., Harvati, K., 2017. Testing modern
human Out-of-Africa dispersal models using dental nonmetric data. Curr.
Anthropol. 58, S406eS417.
Rieseberg, L.H., 1995. The role of hybridization in evolution: Old wine in new skins.
Am. J. Bot. 82, 944e953.
Rieseberg, L.H., 1997. Hybrid origins of plant species. Annu. Rev. Ecol. Systemat. 28,
359e389.
Ripamonti, U., Petit, J.C., Thackeray, J.F., 1999. A supernumerary tooth in a 1.7
million-year-old Australopithecus robustus from Swartkrans, South Africa. Eur. J.
Oral Sci. 107, 317e321.
Ríos, L., Kivell, T.L., Lalueza-Fox, C., Estalrrich, A., García-Tabernero, A., Huguet, R.,
Quintino, Y., de la Rasilla, M., Rosas, A., 2019. Skeletal anomalies in the Nean-
dertal family of El Sidro n (Spain) support a role of inbreeding in Neandertal
extinction. Sci. Rep. 9, 1697.
Roberts, H.F., 1919. Darwin's contribution to the knowledge of hybridization. Am.
Nat. 53, 535e554.
Robinson, J.T., 1954. Prehominid dentition and hominid evolution. Evolution 8,
324e334.
Robinson, J.T., Steudel, K., 1973. Multivariate discriminant analysis of dental data
bearing on early hominid affinities. J. Hum. Evol. 2, 509e527.
Roff, D.A., 1995. The estimation of genetic correlations from phenotypic correla-
tions: A test of Cheverud's conjecture. Heredity 74, 481e490.
Rolian, C., Lieberman, D.E., Hallgrímsson, B., 2010. The coevolution of human hands
and feet. Evolution 64, 1558e1568.
Roseman, C.C., 2004. Detecting interregionally diversifying natural selection on
modern human cranial form by using matched molecular and morphometric
data. Proc. Natl. Acad. Sci. USA 101, 12824e12829.
20
Journal of Human Evolution 174 (2023) 103296
Roseman, C.C., Willmore, K.E., Rogers, J., Hildebolt, C., Sadler, B.E., Richtsmeier, J.T.,
Cheverud, J.M., 2010. Genetic and environmental contributions to variation in
baboon cranial morphology. Am. J. Phys. Anthropol. 143, 1e12.
Rossoni, D.M., Assis, A.P.A., Giannini, N.P., Marroig, G., 2017. Intense natural selection
preceded the invasion of new adaptive zones during the radiation of New
World leaf-nosed bats. Sci. Rep. 7, 11076.
Sage, R.D., Heyneman, D., Lim, K.-C., Wilson, A.C., 1986. Wormy mice in a hybrid
zone. Nature 324, 60e63.
Salser, W., 1978. Globin mRNA sequences: Analysis of base pairing and evolutionary
implications. Cold Spring Harbor Symp. Quant. Biol. 42, 985e1002.
Sankararaman, S., Mallick, S., Dannemann, M., Prüfer, K., Kelso, J., P€ aa€bo, S.,
Patterson, N., Reich, D., 2014. The genomic landscape of Neanderthal ancestry in
present-day humans. Nature 507, 354e357.
Savell, K.R.R., Auerbach, B.M., Roseman, C.C., 2016. Constraint, natural selection,
and the evolution of human body form. Proc. Natl. Acad. Sci. USA 113,
9492e9497.
Schluter, D., 1996. Adaptive radiation along genetic lines of least resistance. Evo-
lution 50, 1766e1774.
Schluter, D., Conte, G.L., 2009. Genetics and ecological speciation. Proc. Natl. Acad.
Sci. USA 106, 9955e9962.
Schroeder, L., 2015. The evolution and diversification of Pleistocene Homo. Ph.D.
Dissertation, University of Cape Town.
Schroeder, L., Ackermann, R.R., 2017. Evolutionary processes shaping diversity
across the Homo lineage. J. Hum. Evol. 111, 1e17.
Schroeder, L., Elton, S., Ackermann, R.R., 2022. Skull variation in Afro-Eurasian
monkeys results from both adaptive and non-adaptive evolutionary pro-
cesses. Sci. Rep. 12, 1e12.
Schroeder, L., Roseman, C.C., Cheverud, J.M., Ackermann, R.R., 2014. Characterizing
the evolutionary path(s) to early Homo. PLoS One 9, e114307.
Schroeder, L., von Cramon-Taubadel, N., 2017. The evolution of hominoid cranial
diversity: A quantitative genetic approach. Evolution 71, 2634e2649.
Seehausen, O., 2004. Hybridization and adaptive radiation. Trends Ecol. Evol. 19,
198e207.
Simon, M.N., Machado, F.A., Marroig, G., 2016. High evolutionary constraints limited
adaptive responses to past climate changes in toad skulls. Proc. R. Soc. B 283,
20161783.
Simonti, C.N., Vernot, B., Bastarache, L., Bottinger, E., Carrell, D.S., Chisholm, R.L.,
Crosslin, D.R., Hebbring, S.J., Jarvik, G.P., Kullo, I.J., Li, R., Pathak, J., Ritchie, M.D.,
Roden, D.M., Verma, S.S., Tromp, G., Prato, J.D., Bush, W.S., Akey, J.M., Denny, J.C.,
Capra, J.A., 2016. The phenotypic legacy of admixture between modern humans
and Neandertals. Science 351, 737e741.
Simpson, G.G., 1953. The Major Features of Evolution. Columbia University Press,
New York.
Siska, V., 2019. Human population history and its interplay with natural selection.
Ph.D. Dissertation, University of Cambridge.
Skovrind, M., Castruita, J.A.S., Haile, J., Treadaway, E.C., Gopalakrishnan, S.,
Westbury, M.V., Heide-Jørgensen, M.P., Szpak, P., Lorenzen, E.D., 2019. Hybrid-
ization between two high Arctic cetaceans confirmed by genomic analysis. Sci.
Rep. 9, 7729.
Slon, V., Mafessoni, F., Vernot, B., de Filippo, C., Grote, S., Viola, B., Hajdinjak, M.,
Peyregne, S., Nagel, S., Brown, S., Douka, K., Higham, T., Kozlikin, M.B.,
Shunkov, M.V., Derevianko, A.P., Kelso, J., Meyer, M., Prüfer, K., Pa €a€bo, S., 2018.
The genome of the offspring of a Neanderthal mother and a Denisovan father.
Nature 561, 113e116.
Smith, H.F., 2009. Which cranial regions reflect molecular distances reliably in
humans? Evidence from three-dimensional morphology. Am. J. Hum. Biol. 21,
36e47.
Smith, H.F., 2011. The role of genetic drift in shaping modern human cranial evo-
lution: A test using microevolutionary modeling. Int. J. Evol. Biol. 2011, 145262.
Smith, F.H., Lacy, K.M., Caldwell, S.J., 2015. Morphological evidence for modern
human influences in Late Central European Neandertals. Anthropologie 53,
61e76.
Sodini, S.M., Kemper, K.E., Wray, N.R., Trzaskowski, M., 2018. Comparison of geno-
typic and phenotypic correlations: Cheverud's conjecture in humans. Genetics
209, 941e948.
Soficaru, A., Doboş, A., Trinkaus, E., 2006. Early modern humans from the Peştera
Muierii, Baia de Fier, Romania. Proc. Natl. Acad. Sci. USA 103, 17196e17201.
Stebbins, G.L., 1950. Variation and Evolution in Plants. Columbia University Press,
New York.
Stebbins, G.L., 1959. The role of hybridization in evolution. Proc. Am. Philos. Soc. 103,
231e251.
Stojanowski, C.M., Paul, K.S., Seidel, A.C., Duncan, W.N., Guatelli-Steinberg, D., 2018.
Heritability and genetic integration of anterior tooth crown variants in the
South Carolina Gullah. Am. J. Phys. Anthropol. 167, 124e143.
Stojanowski, C.M., Paul, K.S., Seidel, A.C., Duncan, W.N., Guatelli-Steinberg, D., 2019.
Quantitative genetic analyses of postcanine morphological crown variation. Am.
J. Phys. Anthropol. 168, 606e631.
Stringer, C., 2012. What makes a modern human. Nature 485, 33e35.
Stringer, C.B., Andrews, P., 1988. Genetic and fossil evidence for the origin of modern
humans. Science 239, 1263e1268.
L. Schroeder and R.R. Ackermann
Stynder, D.D., Brock, F., Sealy, J.C., Wurz, S., Morris, A.G., Volman, T.P., 2009. A mid-
Holocene AMS 14C date for the presumed upper Pleistocene human skeleton
from Peers Cave, South Africa. J. Hum. Evol. 56, 431e434.
Sykes, R.W., 2020. Kindred: Neanderthal Life, Love, Death and Art. Bloomsbury
Publishing, London.
Tattersall, I., Schwartz, J.H., 1999. Hominids and hybrids: The place of Neanderthals
in human evolution. Proc. Natl. Acad. Sci. USA 96, 7117e7119.
Taylor, A.B., Zanolli, C., 2022. Celebrating 50 years of the journal of human evolu-
tion. J. Hum. Evol. 162, 103120.
Taylor, S.A., Larson, E.L., 2019. Insights from genomes into the evolutionary
importance and prevalence of hybridization in nature. Nat. Ecol. Evol. 3,
170e177.
Thorne, A.G., Wolpoff, M.H., 1981. Regional continuity in Australasian Pleistocene
hominid evolution. Am. J. Phys. Anthropol. 55, 337e349.
Thorpe, R.S., Leamy, L., 1983. Morphometric studies in inbred and hybrid house
mice (Mus sp.): Multivariate analysis of size and shape. J. Zool. 199, 421e432.
Tran, C.N.H., Schroeder, L., 2021. Common evolutionary patterns in the human nasal
region across a worldwide sample. Am. J. Phys. Anthropol. 176, 422e433.
Trinkaus, E., 2018. An abundance of developmental anomalies and abnormalities in
Pleistocene people. Proc. Natl. Acad. Sci. USA 115, 11941e11946.
Trinkaus, E., Constantin, S., Zilha~o, J., 2013. Life and Death at the Peştera cu Oase: A
Setting for Modern Human Emergence in Europe. Oxford University Press,
Oxford.
van der Valk, T., Díez-del-Molino, D., Marques-Bonet, T., Guschanski, K., Dale n, L.,
2019. Historical genomes reveal the genomic consequences of recent popula-
tion decline in eastern gorillas. Curr. Biol. 29, 165e170..
Vernot, B., Akey, J.M., 2014. Resurrecting surviving Neandertal lineages from
modern human genomes. Science 343, 1017e1021.
Villanea, F.A., Schraiber, J.G., 2019. Multiple episodes of interbreeding between
Neanderthal and modern humans. Nat. Ecol. Evol. 3, 39e44.
von Cramon-Taubadel, N., 2009. Congruence of individual cranial bone morphology
and neutral molecular affinity patterns in modern humans. Am. J. Phys.
Anthropol. 140, 205e215.
von Cramon-Taubadel, N., 2019. Multivariate morphometrics, quantitative genetics,
and neutral theory: Developing a “modern synthesis” for primate evolutionary
morphology. Evol. Anthropol. 28, 21e33.
von Cramon-Taubadel, N., Lycett, S.J., 2008. Brief communication: Human cranial
variation fits iterative founder effect model with African origin. Am. J. Phys.
Anthropol. 136, 108e113.
von Cramon-Taubadel, N., Schroeder, L., 2018. Quantitative genetics. In:
Trevathan, W. (Ed.), The International Encyclopedia of Biological Anthropology.
John Wiley & Sons, Hoboken, pp. 1e6.
vonHoldt, B.M., Kays, R., Pollinger, J.P., Wayne, R.K., 2016. Admixture mapping
identifies introgressed genomic regions in North American canids. Mol. Ecol. 25,
2443e2453.
vonHoldt, B.M., Pollinger, J.P., Lohmueller, K.E., Han, E., Parker, H.G., Quignon, P.,
Degenhardt, J.D., Boyko, A.R., Earl, D.A., Auton, A., Reynolds, A., Bryc, K.,
Brisbin, A., Knowles, J.C., Mosher, D.S., Spady, T.C., Elkahloun, A., Geffen, E.,
Pilot, M., Jedrzejewski, W., Greco, C., Randi, E., Bannasch, D., Wilton, A.,
Shearman, J., Musiani, M., Cargill, M., Jones, P.G., Qian, Z., Huang, W., Ding, Z.-L.,
Zhang, Y., Bustamante, C.D., Ostrander, E.A., Novembre, J., Wayne, R.K., 2010.
21
Journal of Human Evolution 174 (2023) 103296
Genome-wide SNP and haplotype analyses reveal a rich history underlying dog
domestication. Nature 464, 898e902.
Wang, K., Goldstein, S., Bleasdale, M., Clist, B., Bostoen, K., Bakwa-Lufu, P., Buck, L.T.,
Crowther, A., De me, A., McIntosh, R.J., Mercader, J., Ogola, C., Power, R.C.,
Sawchuk, E., Robertshaw, P., Wilmsen, E.N., Petraglia, M., Ndiema, E.,
Manthi, F.K., Krause, J., Roberts, P., Boivin, N., Schiffels, S., 2020. Ancient ge-
nomes reveal complex patterns of population movement, interaction, and
replacement in sub-Saharan Africa. Sci. Adv. 6, eaaz0183.
Warren, K.A., Ritzman, T.B., Humphreys, R.A., Percival, C.J., Hallgrímsson, B.,
Ackermann, R.R., 2018. Craniomandibular form and body size variation of first
generation mouse hybrids: A model for hominin hybridization. J. Hum. Evol.
116, 57e74.
Weaver, T., 2018. Neutral theory and the evolution of human physical form: An
introduction to models and applications. J. Anthropol. Sci. 96, 7e26.
Weaver, T.D., Gunz, P., 2018. Using geometric morphometric visualizations of
directional selection gradients to investigate morphological differentiation.
Evolution 72, 838e850.
Weaver, T.D., Roseman, C.C., Stringer, C.B., 2007. Were neandertal and modern hu-
man cranial differences produced by natural selection or genetic drift? J. Hum.
Evol. 53, 135e145.
Willmore, K.E., Roseman, C.C., Rogers, J., Cheverud, J.M., Richtsmeier, J.T., 2009.
Comparison of mandibular phenotypic and genetic integration between baboon
and mouse. Evol. Biol. 36, 19e36.
White, T.D., Johanson, D.C., 1982. Pliocene hominid mandibles from the Hadar
Formation, Ethiopia: 1974e1977 collections. Am. J. Phys. Anthropol. 57,
501e544.
Wolpoff, M.H., 1971. Competitive exclusion among Lower Pleistocene hominids: The
single species hypothesis. Man 6, 601e614.
Wolpoff, M.H., Caspari, R., 2000. The many species of humanity. Anthropol. Rev. 63,
3e17.
Wolpoff, M.H., Wu, X., Thorne, A.G., 1984. In: Smith, F.H., Spencer, F. (Eds.), The
Origins of Modern Humans: A World Survey of the Fossil Evidence, 6. Alan R.
Liss, New York, pp. 411e483.
Wood, B.A., McRae, R.T., 2021. Human evolution: Overview. In: eLS. John Wiley &
Sons, Hoboken, pp. 905e913.
Wright, S., 1931. Evolution in Mendelian populations. Genetics 16, 97e159.
Wright, S., 1932. The roles of mutation, inbreeding, crossbreeding, and selection in
evolution. Proc. 6th Intl. Cong. Genet. 1, 356e366.
Wright, S., 1970. Random drift and the shifting balance theory of evolution. In:
Kojima, K. (Ed.), Mathematical Topics in Population Genetics, Biomathematics.
Springer, Berlin, Heidelberg, pp. 1e31.
Yu, N., Jensen-Seaman, M.I., Chemnick, L., Ryder, O., Li, W.-H., 2004. Nucleotide
diversity in gorillas. Genetics 166, 1375e1383.
Zdjelar, N., Nagendran, L., Kendall, C., Ackermann, R.R., Schroeder, L., 2021. The
hybrid skull of the eastern coyote (Canis latrans var.): Nonmetric traits and
craniomandibular shape. J. Morphol. 282, 1745e1764.
Zuckerkandl, E., Pauling, L., 1965a. Evolutionary divergence and convergence in
proteins. In: Bryson, V., Vogel, H.J. (Eds.), Evolving Genes and Proteins. Aca-
demic Press, New York, pp. 97e166.
Zuckerkandl, E., Pauling, L., 1965b. Molecules as documents of evolutionary history.
J. Theor. Biol. 8, 357e366.