DOI: 10.1002/ajpa.

23388

AJPA YEARBOOK ARTICLE

Developments in development: What have we learned from

primate locomotor ontogeny?

Jesse W. Young1 | Liza J. Shapiro2

1
Department of Anatomy and Neurobiology,
Northeast Ohio Medical University
(NEOMED), Rootstown, Ohio, 44272
2
Department of Anthropology, University of
Texas, Austin, Texas, 78712
Correspondence
Jesse W. Young, Department of Anatomy
and Neurobiology, Northeast Ohio Medical
University, 4209 State Route 44,
P.O. Box 95, Rootstown, OH 44272
Email: jwyoung@neomed.edu
Funding information
National Science Foundation, Grant/Award
Numbers: NSF BCS-0313821 and NSF
BCS-0647402; L.S.B. Leakey Foundation
Abstract
The importance of locomotion to evolutionary fitness has led to extensive study of primate loco-
motor behavior, morphology and ecology. Most previous research has focused on adult primates,
but in the last few decades, increased attention to locomotor development has provided new
insights toward our broader understanding of primate adaptation and evolution. Here, we review
the contributions of this body of work from three basic perspectives. First, we assess possible
determinants on the timing of locomotor independence, an important life history event. Significant
influences on timing of locomotor independence include adult female body mass, age at weaning,
and especially relative brain size, a significant predictor of other primate life history variables. Addi-
tionally, we found significant phylogenetic differences in the timing of locomotor independence,
even accounting for these influences. Second, we discuss how structural aspects of primate growth
may enhance the locomotor performance and safety of young primates, despite their inherent neu-
romotor and musculoskeletal limitations. For example, compared to adults, growing primates have
greater muscle mechanical advantage, greater bone robusticity, and larger extremities with rela-
tively long digits. Third, focusing on primate quadrupedalism, we provide examples that illustrate
how ontogenetic transitions in morphology and locomotion can serve as a model system for test-
ing broader principles underlying primate locomotor biomechanics. This approach has led to a
better understanding of the key features that contribute to primates’ stride characteristics, gait
patterns, limb force distribution, and limb postures. We have learned a great deal from the study
of locomotor ontogeny, but there is much left to explore. We conclude by offering guidelines for
future research, both in the laboratory and the field.

KEYWORDS
allometry, gait mechanics, life history, locomotor independence, ontogeny

1 | INTRODUCTION and morphological underpinnings of primate locomotor behaviors have

Primates display an impressively broad range of locomotor behaviors,
including several highly charismatic and unique behaviors not seen in
other mammals, such as strepsirrhine vertical clinging and leaping, hylo-
batid brachiation, and hominin striding bipedalism (Fleagle, 2013; Hunt
et al., 1996; Schmitt, 2010). Even primate quadrupedal locomotion, a
comparatively ubiquitous locomotor mode, is characterized by several
unique features relative to most other mammalian quadrupeds (Kimura,
1992; Kimura, Okada, & Ishida, 1979; Larson, 1998; Schmitt, 2010;
Shapiro & Young, 2016). As such, the biomechanics, ecological context,
Jesse W. Young and Liza J. Shapiro contributed equally to this work.
long been of interest in anthropology and associated fields (Dagosto &
& Gebo, 1998; Le Gros Clark, 1959; Muybridge, 1887; Napier, 1967;
Prost, 1965; Ripley, 1967; Wood Jones, 1916).
The vast majority of previous research on primate locomotion,
whether in the field or the lab, has concentrated on adult animals. To
some degree, this focus on adults is understandable. The morphological
and behavioral changes that occur during ontogeny add an additional
layer of variability that may obscure relationships of interest (e.g., asso-
ciations between substrate size and positional behavior) (Jones & Ger-
man, 2005). Additionally, from an evolutionary point of view,
reproduction—and thus gene transmission—is by definition limited to
sexually mature adult animals. However, over the lifespan evolutionary

Am J Phys Anthropol. 2018; 165: 37–71 wileyonlinelibrary.com/journal/ajpa V

C 2018 American Association of Physical Anthropologists | 37
38 | YOUNG
fitness is predicated on an individual’s ability to clear two fundamental
life history “hurdles”: surviving to reproductive age and reproducing
successfully (Jones, 2011). Because infants and juveniles have yet to
reach reproductive age, any feature of an immature animal’s biology
that promotes or limits survival has the potential to be a fitness-critical
trait, and thus of interest to researchers interested in primate adapta-
tion and evolution.
Almost 30 years ago, Hurov (1991) published a paper entitled
“Rethinking Primate Locomotion: What can we learn from develop-
ment?” Hurov outlined how studies of locomotor development can
provide unique insights toward our understanding of the functional
morphology and evolution of primate locomotor adaptation. As
expressed by Hurov, the unique value of developmental studies lies in
the fact that “changes in the physical properties of the musculoskeletal
system during growth represent a unique natural manipulative experi-
ment in which hypotheses of correlated change in performance, sub-
strate selection, and structural design can be tested for their causal
relationships” (Hurov, 1991:212). Hurov (1991) framed several broad
areas of inquiry regarding growth and locomotor behavior, and high-
lighted the many gaps in our knowledge in these areas at that time.
Since 1991, there has been a substantial improvement in our under-
standing of primate locomotor development. In this article, we set out
to answer Hurov’s call for research by addressing what we have
learned from developmental locomotor studies of primates in the past
several decades.
Here, we broadly review existing literature on primate locomotor
development from a functional perspective. Our review is divided into
three sections. First, we discuss locomotor development in a life history
context, seeking to understand possible functional relationships
between the timing of locomotor independence and other aspects of
an individual’s development and ecology. We focus on early develop-
ment and the transition to locomotor independence. Other recent
reviews have focused on associations between the positional behavior
of juvenile primates and life history (Bezanson, 2017; Bezanson & Mor-
beck, 2013). Second, we review possible functional influences on pri-
mate postcranial growth, specifically addressing how ontogenetic
changes in body size, muscle leverage, relative bone strength, and
grasping capacity may be associated with the unique ecological pres-
sures faced by immature animals. Third, we discuss how integrated
studies of primate growth and locomotor development can be used as
a model system to understand broader principles of primate locomotor
biomechanics, focusing on the mechanics of primate quadrupedalism.
We argue that the increased morphological and behavioral variability
inherent to studies of locomotor ontogeny are actually a beneficial
“feature” of the system, rather than a “bug.” Finally, we articulate some
general guidelines for future studies of primate locomotor
development.
2 | PRIMATE LOCOMOTOR DEVELOPMENT
AND LIFE HISTORY
As a discipline, life history research aims to define a succinct set of
parameters that determine an individuals’ lifetime reproductive success
ET AL.
(Kappeler, Pereira, & van Schaik, 2003; Leigh & Blomquist, 2007;
Stearns, 1992). Understanding the patterns and determinants of life
history variation therefore can provide a critical window into the evolu-
tionary process. Comparative studies of primate life history are well-
represented in the literature (Barrickman, Bastian, Isler, & Van Schaik,
2008; Garber & Leigh, 1997; Harvey & Clutton-Brock, 1985; Kamilar &
Cooper, 2013; Kappeler, 1998; Leigh, 2004; Leigh & Terranova, 1998;
Pontzer et al., 2014; Shattuck & Williams, 2010; Sibly & Brown, 2007;
Tilden & Oftedal, 1997). A common theme to these studies has been
the finding that primate life histories are “slow” relative to other mam-
mals (Harvey, Martin, & Clutton-Brock, 1987). For example, primates
are characterized by late ages of weaning and sexual maturity, slow
postnatal growth rates, and long life spans relative to other mammals
of similar size (Austad & Fischer, 1992; Barrickman et al., 2008; Case,
1978; Charnov, 1993; Kirkwood, 1985; Lee, Maijuf, & Gordon, 1991;
Pereira & Fairbanks, 1993; Pontzer et al., 2014; Ross, 1998). Taken
together, these data indicate that primates experience relatively and
absolutely longer periods of nonreproductive infancy and juvenility.
Few studies, however, have explicitly considered locomotor develop-
ment as a critical life history parameter unto itself (but see Bezanson,
2009; Bezanson & Morbeck, 2013; Zihlman, 1992).
Primate infants are born behaviorally (or secondarily) altricial (Port-
mann, 1958), and are generally not able to support their own weight or
effect their own movement at birth (Grand, 1992; Kappeler et al.,
2003). During this early period of “locomotor dependence,” most
infants are transported by their mother or another caregiver during for-
aging and travel, typically by clinging to either their venter or the dor-
sum, though strepsirrhines will transport infants orally as well as “park”
infants in nests, tree holes, or other refugia (Kappeler, 1998; Ross,
2001). Both theoretical models and empirical data suggest that infant
carrying is costly to the carrier (Altmann & Samuels, 1992; Kramer,
1998; Nicolson, 1987; Pontzer & Wrangham, 2006; Ross, 2001; Tardif,
1994; Tecot, Baden, Romine, & Kamilar, 2012a). For example, male
cotton-top tamarins (Saguinus oedipus) lose body mass and exhibit
lower average travel speeds during periods of infant transport
(Caperos, Morcillo, Pel
aez, Fidalgo, & S
anchez, 2012; S

anchez, Pel
aez,
€rmann, & Kaumanns, 1999). Infant carrying compromises forag-
Gil-Bu
ing efficiency in saddle-back tamarins (Saguinus fuscicollis), vervet mon-
keys (Chlorocebus aethiops), and siamangs (Symphalangus syndactulus)
(Goldizen, 1987; Lappan, 2009; Whitten, 1982). Similarly, female squir-
rel monkeys (Saimiri collinsi) limit their time spent travelling during the
lactational period, perhaps to reduce the energetic burden of carrying a
relatively large, fast growing infant (Garber & Leigh, 1997; Ruivo,
Stone, & Fienup, 2017). Experimental data show that carrying a mass
equivalent to that of a newborn litter significantly compromises leaping
performance in common marmosets (Callithrix jacchus) (Schradin &
Anzenberger, 2001), reducing leaping distance by an average of 17%.
Similarly, spectral tarsier (Tarsier tarsier) mothers significantly reduce
vertical clinging and leaping locomotor behaviors when carrying infants,
instead switching to arboreal quadrupedalism as the primary form of
locomotion (Gursky, 2007). Finally, across strepsirrhine primates, spe-
cies that carry infants—rather than park them in refugia—have signifi-
cantly smaller home ranges, wean their infants at relatively later ages,
YOUNG ET AL.
and begin reproduction at relatively late ages (Ross, 2001). Ross (2001)
argues that the increased energetic burden of infant carrying accounts
for the relative rarity of continuous infant transport across mammals
(see also Nicolson, 1987). Such energetic costs can indeed be substan-
tial, particularly for small primates. For instance, based on long-term
field studies of infant care in spectral tarsiers—a nocturnal haplorrhine
that typically parks, or “caches,” infants in trees during nighttime forag-
ing—Gursky (2003, 2007) calculated that should a tarsier mother
instead choose to continuously carry her infant, the extra foraging time
required to compensate for the energetic deficit would exceed the
available hours in the night. Although transport costs to the mother
may be relieved in species characterized by nonmaternal infant care
(i.e., allomothering; Hrdy, 1976), the costs discussed above would also
necessarily accrue to any caretaker, whether the mother or another
individual, again suggesting an energetic burden to carrying dependent
infants.
In summary, given that carrying infants is energetically costly, rapid
locomotor independence would seem to be beneficial to the caregiver,
though not necessarily to the progeny. The transition to locomotor
independence can be viewed as another case of “parent-offspring con-
flict,” akin to the better studied phenomenon of nutritional independ-
ence (i.e., weaning: Maestripieri, 2002; Trivers, 1974). However, the
dynamics of the transition to locomotor independence are more com-
plex than would be reflected in a simple “early locomotion is always
better” rule. Additional parameters must be considered in this transi-
tion. For example, if lactating mothers still provide nutritional support
to an independently moving infant, the mother must still ingest suffi-
cient resources to cover the infant’s energetic cost of transporting itself
(Kramer, 1998). The energetic burden of providing for an independent
infant could therefore be greater than the cost of simply carrying the
infant, as suggested by Altmann and Samuels (1992). In this study, an
extensive dataset on infant growth and development in yellow baboons
(Papio cynocephalus) was used to examine how maternal energetics are
impacted by the interplay of these two forces (i.e., transporting a
dependent infant versus supplementing an independent one). Their
data suggest that transporting infants is always energetically cheaper
than providing nutritional support to an independent one, given that
the nutritional needs of a passive infant will always necessarily be less
than those of an active one. However, as noted by Gurksy (2003), the
model used in the Altmann and Samuels (1992) study did not include
the additional energetic cost to the mother of supporting the infant’s
mass. Oxygen-consumption studies have shown that carrying a load
increases the cost of transport in direct proportion to the mass-specific
magnitude of the load (i.e., adding a load equal to 10% of body mass
would increase the cost of transport by 10%: Bastien, Willems,
Schepens, & Heglund, 2005; Taylor, Heglund, McMahon, & Looney,
1980; Wickler, Hoyt, Cogger, & Hall, 2001). Using the growth rate
model established for this baboon population (Altmann & Alberts,
1987), we calculated the average monthly mass of a baboon infant
through the first year of life, and used these estimated values to calcu-
late the additional energetic cost to the mother of moving under this
load. If the energetic expenditure of infant transport is modified to
include the effects of supporting the infant’s mass, a transition point
| 39
FIGURE 1 A modified version of Figure 5 from Altmann and
Samuels (1992), illustrating the additional energetic cost to a
baboon mother under two scenarios: if the mother provided all
infant transport (open circles), or if the infant provided all transport
by walking on its own (closed black triangles). Closed red circles
illustrate the additional cost of infant transport inclusive of the
cost of supporting the infant’s mass. Note that infant transport
becomes more expensive than supporting an independent infant at
approximately eight months of age, the age of yellow baboon
locomotor independence (Altmann, 1980).
occurs at eight months of age, where the cost of carrying becomes
greater than the cost of providing nutritional support to an independ-
ent infant (Figure 1). Eight months is also the typical age of locomotor
independence in wild yellow baboons (Altmann, 1980).
Existing data therefore suggest that the developmental transition
to locomotor independence likely reflect a dynamic interplay between
several competing factors. In an effort to investigate the determinants
of locomotor development more broadly across primates, we reviewed
primary literature on wild primate development to find modal ages at
which infants achieved locomotor independence (Table 1). Only data
from field studies of primates moving in their natural habitats were
included. Because locomotor independence, like nutritional independ-
ence, is a protracted developmental process rather than a binary event
(Lee, 1996; Nicolson, 1987), we operationally declared infants to be
independent once they depended on carrying for no more than 20% of
their daily transport. We were ultimately able to identify ages of loco-
motor independence for a total of 37 primate species, including nine
strepsirrhine taxa (one cheirogaleid, two lemurids, three indriids, two
galagids, and one lorisid) and 28 haplorrhine taxa (one tarsiid, one
aotine, six callitrichines, four cebines, five atelids, five cercopithecids,
and six nonhuman hominids) (Table 1; Figure 2). To test for possible
correlations between age at locomotor independence and other
aspects of primate biology, we merged these data with a database of
eight other variables characterizing developmental, morphological, and
ecological variation across the primates in our sample, extracted from
existing comparative primate databases or from primary literature
40 | YOUNG ET AL.

(Table 1). Wherever possible, we strove to select life history data from 2.1 | Analytical methods
wild populations, given the degree to which captive provisioning can
All variables were log-transformed prior to analysis. We used multiple
impact growth and development. Specific variables included adult
phylogenetic generalized least squares (PGLS) regression to test for
female body mass, age at weaning, neonatal body mass, postnatal
bivariate relationships between age at locomotor independence and
growth rate, adult female endocranial volume (a validated proxy for
most of the continuous predictor variables. Female body mass was
brain size: Isler, Kirk, & Miller, 2008), daily path length, and modal sub-
entered as a second predictor variable representing body size, such
strate preference (i.e., arboreal or terrestrial). We discuss our logic for
that the partial regression coefficient between the predictor of interest
selecting these specific predictors below, as we review each of our
and age at locomotor independence represents the bivariate
findings.

T AB LE 1 Comparative dataset used to investigate the determinants of locomotor independence across primatesa.

Species Loco Ind Fem mass Wean Neo mass Growth rate ECV DPL Sub Sources

Otolemur crassicaudatus 45 1.11 135 44 10.16 11.06 1.25 A LI [11]; DPL [56]

Galago senegalensis 35 0.22 98 19 1.75 3.90 2.10 A LI [11]; DPL [48]

Perodicticus potto 183 0.84 151 36 4.73 11.87 A LI [9]

Varecia variegata 91 3.52 90 89 1.95 31.17 1.13 A LI [7, 36]; DPL [56]

Lemur catta 112 2.21 142 79 9.15 19.75 0.95 T LI [22]; DPL [35]

Propithecus diadema 213 6.26 273 135 40.51 0.99 A LI [60]; DPL [25]

Propithecus verreauxi 183 2.95 182 103 24.92 0.85 A LI [43]; DPL [40]

Propithecus coquereli 175 4.28 182 103 0.73 A LI [45, 57]; DPL [32]
c c
Microcebus rufus 61 0.043 40 6 1.35 1.80 A LI [4]

Tarsius tarsier 58 0.106 80 24 0.43 3.22 0.48 A LI, DPL [23]

Saimiri oerstedii 152 0.68 112 25.52 3.35 A LI [6]; DPL [35]

Sapajus apella 243 2.52 314 215 2.87 64.32 2.00 A LI [16]; DPL [40]

Cebus capucinus 183 2.54 514 240 2.17 72.12 2.00 A LI [5, 31]; DPL [40]

Cebus olivaceus 228 2.52 730 68.38 2.14 A LI [58]; DPL [44]

Saguinus fuscicollis 76 0.36 90 39 8.03 1.32 A LI [51, 53]; DPL [40]

Saguinus oedipus 84 0.4 50 43 3.50 9.92 1.37 A LI [24]; DPL [40]

Saguinus geoffroyi 61 0.5 56 48 10.19 2.06 A LI [51]; DPL [12]

Callithrix jacchus 42 0.38 76 29 2.98 7.05 1.11 A LI [52]; DPL [13]

Callithrix flaviceps 91 0.41 1.22 A LI [18]; DPL [17];

Cebuella pygmaea 56 0.12 90 13 0.90 0.29 A LI [51]; DPL [56]

Aotus trivirgatus 91 0.74 127 94 3.50 16.13 0.25 A LI [59]; DPL [35]
b b
Lagothrix poeppigii 730 4.53 411 440 98.00 1.84 A LI [49]; DPL [19]

Ateles paniscus 365 8.44 785 453 4.39 101.20 2.70 A LI [55]; DPL [40]

Alouatta guariba 152 4.55 365 49.08 0.75 A LI, W [34, 39]; DPL [1]

Alouatta seniculus 274 5.3 372 295 3.50 54.26 0.58 A LI [30]; DPL [35]

Alouatta palliata 183 5.32 483 320 1.36 48.04 0.39 A LI [10, 42]; DPL [40]

Pongo pygmaeus 1644 35.8 1274 1691 7.26 337.72 0.50 A LI [33]; DPL [40]

Pongo abelii 1096 35.6 2557 341.21 A LI [54]

Pan troglodytes 1826 41.6 1736 1782 3.97 350.54 2.10 T LI [14, 15, 47]; DPL [41]

Pan paniscus 1826 33.2 1087 1447 6.71 326.25 1.80 T LI [14, 15]; DPL [40]

Gorilla gorilla 1461 71.5 1061 2053 15.32 455.89 0.70 T LI [8]; DPL [56]
(Continues)
YOUNG ET AL. | 41

T AB LE 1 (Continued)

Species Loco Ind Fem mass Wean Neo mass Growth rate ECV DPL Sub Sources

Gorilla beringei 913 97.5 1278 480.15 0.35 T LI [15]; DPL [35]

Macaca mulatta 152 5.37 293 470 4.39 84.26 1.43 T LI [29]; DPL [35]

Papio cynocephalus 243 12.3 424 757 5.10 156.13 5.50 T LI [2, 3]; DPL [35]

Papio anubis 335 13.3 592 480 152.45 2.01 T LI [37]; DPL [35]

Chlorocebus aethiops 91 4.09 283 383 4.20 59.00 0.95 T LI [28]; DPL [40]

Chlorocebus aethiops 91 4.09 283 383 4.20 59.00 0.95 T LI [28]; DPL [40]
a
Table headings. Loco ind: age at locomotor independence (in days); Fem mass: adult female body mass (in kilograms [50]); Wean: weaning age/lacta-
tional duration (in days [27]); Neo mass: neonatal body mass (in grams [27]); growth rate: postnatal growth rate of the litter (in grams/day [27, 46]);
ECV: endocranial volume (in cm3 [26]); DPL: daily path length (in kilometers); Sub: modal substrate (A: arboreal or T: terrestrial [20, 38]), Sources:
LI 5 source(s) for locomotor independence data, DPL: source for daily path length. Missing values in any column are left blank.
b
Neonatal body mass and endocranial volume are for Lagothrix lagothricha.
c
Growth rate and endocranial volume are for Microcebus murinus.
SOURCES
[1] Agostini, Holzmann, and Di Bitetti (2010); [2] Altmann (1980); [3] Altmann and Samuels (1992); [4] Atsalis (2015); [5] Bezanson (2006); [6] Boinski
and Fragaszy (1989); [7] Boskoff (1977); [8] Breuer, Hockemba, Olejniczak, Parnell, & Stokes (2008); [9] Charles-Dominique (1977); [10] Clarke (1990);
[11] Crompton (1983); [12] Dawson (1979); [13] Digby and Barreto (1996); [14] Doran (1992); [15] Doran (1997); [16] Escobar-P
aramo (1989);
€ rster and Cords (2002); [22] Gould (1990); [23] Gursky (2007);
[17] Ferrari (1988); [18] Ferrari (1992); [19] Fiore (2003); [20] Fleagle (2013); [21] Fo
[24] Hershkovitz (1977); [25] Irwin (2007); [26] Isler et al. (2008); [27] Kappeler and Pereira (2003); [28] Lancaster (1971); [29] Lindburg (1971); [30]
Mack (1979); [31] MacKinnon (1995); [32] McGoogan (2011); [33] Mendonça et al. (2016); [34] Miranda, Aguiar, Ludwig, Moro-Rios, & Passos (2005);
[35] Mitani and Rodman (1979); [36] Morland (1990); [37] Nash (1978); [38] Nunn and Barton (2001); [39] Podgaiski and de Assis Jardim (2009); [40]
Pontzer and Kamilar (2008); [41] Pontzer and Wrangham (2006); [42] Raguet-Schofield and Pave
(2014); [43] Richard (1976); [44] Robinson (1986); [45]
Ross and Lehman (2016); [46] Ross (1991); [47] Sarringhaus et al. (2014); [48] Schaefer and Nash (2007); [49] Schmitt and Fiore (2014); [50] Smith and
Jungers (1997); [51] Snowdon and Soini (1988); [52] Stevenson and Rylands (1988); [53] Terborgh (1983); [54] van Noordwijk and van Schaik (2005); [55]
van Roosmalen and Klein (1988); [56] Wheeler, Bradley, and Kamilar (2011); [57] Wolf (2011); [58] Wright (2005); [59] Wright (1990); [60] Wright (1995).

association after removing the influence of body size. PGLS regression
accounts for phylogenetic signal in the data by modeling the residual
error variance-covariance structure to reflect the phylogenetic relation-
ships among the represented taxa (Nunn, 2011). The particular covari-
ance structure among residuals can be modified to represent different
models of trait evolution. A model in which the residual error variance
perfectly tracks the branching among taxonomic groups is most often
referred to as a “Brownian Motion” model of evolution. Similar to the
atomic physics concept of random molecular motion, a Brownian
Motion model assumes that phenotypic traits drift randomly over time,
such that trait variance is a function of divergence time across the phy-
logeny. Trait variances are also assumed to be sampled from a normal
distribution with a mean of zero, such that any trait changes are not
specifically directional (i.e., a neutral model of evolution). Rather than
assume a Brownian motion model for PGLS regressions, we employed
an adjusted version of the phylogenetic variance-covariance matrix in
which the off-diagonal elements of the matrix were multiplied by a
scaling parameter (Pagel’s k) that quantifies how closely the covariance
structure matches the expectation under Brownian Motion (Freckleton,
Harvey, & Pagel, 2002; Nunn, 2011). A k value of 1 matches the
assumptions of the Brownian Motion model, whereas a value of 0
matches the assumptions of ordinary least squares regression (i.e.,
uncorrelated residual errors). Intermediate values can be interpreted to
indicate an interplay between phylogenetic signal and selection (Kami-
lar & Cooper, 2013).
We used a different procedure to examine the independent influ-
ence of neonatal body mass and endocranial volume on age at
locomotor independence, controlling for the effect of adult female
body mass. Although it would have been possible to use multiple PGLS
regression for these analyses as well, parameter estimates would have
been unstable due to high collinearity between these morphological
variables and adult female body mass (i.e., collinearity: Graham, 2003).
Variance inflation factors (VIFs) for neonatal body mass and endocra-
nial volume, calculated from PGLS regressions of each measure on
female body mass, were 9.02 and 9.58, respectively, indicating a high
degree of collinearity (VIFs for all other predictor terms were all
2.35)
(Graham, 2003). Therefore, we implemented a phylogenetically con-
trolled ridge regression approach, as recommended by Nunn (2011).
Ridge regression is an extension of the ordinary least squares model
that helps correct for collinearity by biasing regression estimates in
order to reduce their standard errors and improve reliability (Neter,
Kutner, Nachtsheim, & Wasserman, 1996). We first calculated phyloge-
netic independent contrasts of log-transformed age at locomotor inde-
pendence, adult female body mass, and the predictor variable of
interest (i.e., neonatal mass or endocranial volume). Contrasts were
scaled to the square root of summed branch lengths to control for het-
eroscedasticity due to variance in divergence times. It is important to
note that analyses of scaled phylogenetic independent contrasts implic-
itly assume a Brownian Motion model of evolution (Nunn, 2011). How-
ever, because body mass, neonatal mass, and endocranial volume all
displayed relatively high values of k (see results below), and since k 5 1
implies Brownian Motion, an assumption of a Brownian Motion model
of trait evolution was considered reasonable. Scaled contrasts were
transformed to z-scores prior to running the ridge regressions, as the
42 | YOUNG ET AL.

FIGURE 2 Chronogram of the phylogeny used for all PGLS regressions (sampled from the consensus tree of Arnold et al., 2010). Colors
mapped onto the species at the tree tips correspond to family level groupings used for most of subsequent comparative scatterplots below

standard ridge regression algorithm assumes variables are scaled and
centered (Neter et al., 1996). Additionally, all regressions were forced
through the origin (i.e., fit with a zero intercept), a recommended prac-
tice when testing for associations among phylogenetic independent
contrasts (Garland, Harvey, & Ives, 1992).
The primate phylogeny used in all of our comparative analyses
was subsampled from the consensus tree of Arnold, Matthews, and
Nunn (2010) (Figure 2). All statistical analyses were performed in R
statistical package (R Core Team, 2017), with the add-on packages
ape (Paradis, Claude, & Strimmer, 2004), boot (Conty & Ripley,
2009), caper (Orme et al., 2013), GEIGER (Harmon, Weir, Brock,
Glor, & Challenger, 2007), phytools (Revell, 2012), and ridge (Moritz
& Cule, 2017).
2.2 | Phylogenetic signal
Age at locomotor independence ranged from a minimum of 35 days in
lesser bush babies (Galago senegalensis) to 5 years in bonobos and
chimpanzees (Pan paniscus and P. troglodytes) (Table 1). We assessed
the degree of phylogenetic signal in the distribution of locomotor inde-
pendence ages across primates by calculating Blomberg’s K for each
continuous variable in our dataset (Blomberg, Garland, & Ives, 2003).
YOUNG ET AL. | 43

T AB LE 2 Phylogenetic signal in primate developmental, morpholog- neonatal body mass and endocranial volume were characterized by
ical, and ecological traits, as quantified by Blomberg’s K. higher values of K. In a broader analysis of phylogenetic signal across
Trait K p (K > 0) a several primate traits, Kamilar and Cooper (2013) noted that morpho-
logical variables—particularly brain size—tend to high phylogenetic sig-
Age at locomotor independence 0.862 0.001
nal across primates (i.e., K values of 0.670–1.25). In summary, age at
Adult female body mass 0.715 0.001
locomotor independence was phylogenetically conservative across pri-
Age at weaning 0.440 0.01 mate clades, such that if a given species displays a relatively early (or
Neonatal body mass 1.33 0.001 late) age of independence, it is likely that its close relatives will do the

Postnatal growth rate 0.301 0.286

same.

Endocranial volume 2.23 0.001

Daily path length 0.143 0.432
a
Values displaying significant phylogenetic signal, as indicated by a K
value significantly different from zero, are indicated in bold font.
Like k, K quantifies interspecific trait variance relative to the expecta-
tion under a Brownian Motion model of evolution, with K 5 1 indicat-
ing a perfect fit to a Brownian Motion model, K 5 0 indicating
phylogenetic independence at the tree tips, and intermediate values
suggesting a balance between random phenotypic drift and a more
directional evolutionary process. It is also possible for K to be greater
than 1, indicating that close relatives are more similar to one another
than would be expected under a Brownian Motion model (Kamilar &
Cooper, 2013; Nunn, 2011). Across our primate sample, age at locomo-
tor independence displayed a strong phylogenetic signal, with a K value
higher than all but two other variables in the dataset (Table 2). Only
2.3 | Influence of body mass
We predicted that age at locomotor independence will be positively
correlated with body mass, such that larger species will achieve inde-
pendence at later ages. The inverse relationship between body size and
physiological time is well-documented across animals—the pace of life
is slower in larger animals. Fundamental temporal parameters, including
gestation length, age at weaning (i.e., lactation duration), age of first
reproduction, and total lifespan, are all greater in larger animals (Calder,
1984; Lindstedt & Calder, 1981; Schmidt-Nielsen, 1984). Accordingly,
given that locomotor independence should at least partially be depend-
ent on the growth and maturation rate of the infant itself, we predicted
that ages at locomotor independence will increase with body size.
In accordance with our prediction, age at locomotor independence
was significantly positively associated with body mass (Table 3, Figure
3a). Larger species require significantly more time to achieve locomotor
independence than smaller species, with age at locomotor

T AB LE 3 Comparative analyses of developmental, morphological, and ecological influences on age at locomotor independence in primatesa.

Model Summary Effect of predictor Effect of body mass

Pagel’s k
Predictor R2 [95% CI] F DF P Slope P Slope P

Female body mass (kg) 0.394 0.922 22.8 1, 35 <0.001 0.390 <0.001 NA NA
[0.557, 0.999]

Weaning age (days) 0.574 0.799 22.2 2, 33 <0.001 0.497 0.013 0.188 0.105
[0.00, 0.987]

Neonatal massb 0.740 – – – – 0.222 0.082 0.311 0.015

Growth rate 0.463 1.00 9.0 2, 21 0.002 20.021 0.891 0.396 0.001
[0.681, 1.00]

ECV model 1 (cm3)b,c 0.535 – – – – 1.37 <0.001 20.757 0.020

ECV model 2 (cm ) 3 b,c

0.480 – – – – 1.28 0.001 20.697 0.045

Daily path length (km) 0.515 0.852 16.5 2, 31 <0.001 0.115 0.337 0.476 <0.001
[0.342, 0.988]

Modal substrated 0.393 0.924 11.0 2, 34 <0.001 NA 0.820 0.385 <0.001

[0.561, 0.999]
a
Values summarize the effects of phylogenetic generalized least squares regressions of age at locomotor independence on the indicated variables, con-
trolling for the effect of body mass where appropriate using multiple regression. Variable definitions and data sources are summarized in the text. All
continuous variables were log-transformed prior model fitting. Significant terms are indicated by bold text. In this case, Pagel’s k is an index of the phy-
logenetic signal in the regression residuals, not of the dependent variable itself (i.e., age at locomotor independence).
b
As described in the text, the independent influence of these variables on age at locomotor independence, adjusted for the influence of adult female
body mass, was tested using multiple ridge regression of phylogenetic independent contrasts.
c
Following Garwicz et al (2009), endocranial volume (ECV, a proxy for brain size; Isler et al. 2008) is tested as a predictor of locomotor independence in
days of postnatal development (Model 1) as well as time since conception (Model 2).
d
Regression coefficients are not provided for these categorical predictor variables.
44 | YOUNG ET AL.

FIGURE 3 a) Association between age locomotor independence and average adult female body mass. Line indicates PGLS regression fit
(see Table 3 for model parameters). b) Residual age of locomotor independence (after controlling for the effects of female body mass),
expressed as a percentage of the fitted value, grouped by taxonomic family. Abbreviations: Lem 5 Lemuridae, Che 5 Cheirogaleidae,
Ind 5 Indridae, Gal 5 Galagidae, Lor 5 Lorisidae, Tar 5 Tarsiidae, Aot 5 Aotinae, Cal 5 Callitrichinae, Ceb 5 Cebinae, Ate 5 Atelidae,
Cer 5 Cercopithecidae, Hom 5 Hominidae

independence specifically scaling to body mass with negative allometry
(i.e., M0.39). The bootstrapped 95% confidence intervals on this expo-
nent (0.130–0.397) indicate that the relationship between age at loco-
motor independence and body mass is not significantly different from
the common quarter-power scaling trend that characterizes many
physiological durations across mammals, including cardiac cycles, respi-
ratory cycles, gestation periods, and overall life span (Calder 1984;
Lindstedt & Calder 1981).
Nevertheless, comparison of residual variance among primate fam-
ilies shows that not all variation in age at locomotor independence can
be explained by body size alone (Figure 3b). Some groups—such as
correlated with one another, and that on average locomotor independ-
ence should occur prior to weaning.
As predicted, age at locomotor independence was strongly corre-
lated with age at weaning, even after adjusting for the effects of body
mass (Figure 4a). In fact, PGLS regression suggested that adult female
body mass was no longer a significant predictor of variation in locomotor
independence once weaning age was included in the model (Table 3). To
some degree, the lack of significance for the body mass term could be
due to collinearity between the predictor variables, though the variance
inflation factor between weaning age and adult female body mass was
not particularly high (2.35; R2 5 0.575). Moreover, a ridge regression

lemurids, galagids, and cercopithecids—achieve locomotor independ- using scaled independent contrasts also indicated a marginally non-

ence at relatively early stages, whereas others—such as lowland wooly significant relationship between age at locomotor independence and

monkeys (i.e., L. poeppigii, the outlier above the Atelid group) and homi- body mass when weaning age was included in the model (p 5 0.055),

nids—achieve locomotor independence relatively late. Clearly, some
factor independent of body size is required to explain this additional
variation age at locomotor independence.
whereas the effect of weaning age remained significant (p 5 0.021).
These results show that primates who tend to wean at relatively
(or absolutely) late ages also tend to have late ages of locomotor inde-
pendence. However, the two events are not perfectly contemporane-
ous. An investigation of age distributions in Table 1 shows that for

2.4 | Influence of weaning age
Controlling for effects of adult female body mass, we predicted that
age at locomotor independence will be positively correlated with wean-
ing age, such that infants that wean at relatively late ages will also
achieve independence at later ages. We predicted that, in general, the
time course of locomotor independence should parallel that of nutri-
tional independence. Barring food sharing from group mates, a weaned
infant must be able to independently access foraging resources. Simi-
larly, as illustrated above using the baboon example of Altmann and
Samuels (1992) (Figure 1), an independently moving infant should be
expected to provide some of its own nutritional support, lest the lacta-
tional costs to the mother become unwieldy. Therefore, we expected
weaning age and age at locomotor independence to be directly
most species in our database for whom we could identify both weaning
ages and ages at locomotor independence, locomotor independence
occurs prior to weaning (i.e., 24 out of 36 species, or 66%). To investi-
gate the general temporal coordination between weaning and locomo-
tor independence, we used PGLS regression to fit log-transformed ages
at locomotor independence to log-transformed ages at weaning (with-
out including body mass as a predictor term). If the two events are gen-
erally contemporaneous, we would expect the 95% confidence
intervals on both the slope and intercept of the regression equation to
include 1. Logged age at locomotor independence scaled to logged age
at weaning with an intercept of 0.958 and a slope of 0.755 (Figure 4b).
95% confidence intervals about these values (calculated using a boot-
strapping procedure with 10,000 replicates) were 0.828–2.16 for the
intercept and 0.503–0.769 for the slope. These data indicate that if
YOUNG ET AL. | 45

FIGURE 4 a) Partial-regression plot (Quinn & Keough, 2002) of age at locomotor independence versus age at weaning. The trend line indi-
cates the independent association between the two variables, controlling for the effects of adult female body mass and phylogeny using
multiple PGLS. b) Log-log plot of age at locomotor independence against age at weaning. The dashed line indicates the line of identity (i.e.,
age at locomotor independence equal to age at weaning) whereas the solid line indicates the PGLS fit to the data. Note that age at locomo-
tor independence tends to occur earlier than age at weaning, with the pronounced exception of non-human hominoids, where age at
locomotor independence is roughly contemporaneous with age at weaning

locomotor independence and nutritional independence both occur rela-
tively early, the two events are generally contemporaneous. However,
slope values significantly less than 1 indicate a complex allometric rela-
tionship between age at locomotor independence and weaning, such
that locomotor independence tends to occur at relatively earlier ages
as the absolute age at weaning increases. It may be that, due to the
negatively allometric scaling of metabolic rates (i.e., Kleiber’s rule) larger
primate infants—who generally reach locomotor independence at later
ages (Figure 3)—are buffered from energetic concerns that would com-
promise smaller species. Hominids, however, are an exception to this
general pattern, with a late age of locomotor independence matching a
late age of weaning (Figure 4b). Moreover, as discussed above, it must
be remembered that both weaning and locomotor independence are
operationally defined for ease of comparison—neither of these events
are binary processes with definitive ages of occurrence. Ultimately only
detailed longitudinal study of wild primate infants can demonstrate the
underlying covariation between the two processes.
2.5 | Influence of infant body size and growth rate
The metabolic cost of carrying a load generally increases directly in pro-
portion to the load (i.e., carrying a load equal to 10% of body mass will
increase transport costs by 10%: Bastien et al., 2005; Taylor, Heglund,
McMahon, & Looney, 1980; Wickler et al., 2001). Therefore, larger
infants should be more costly to carry (Dunbar, 1988; Kramer, 1998;
Wall-Scheffler, Geiger, & Steudel-Numbers, 2007). Indeed, infant carry-
ing has been shown to compromise leaping in common marmosets and
spectral tarsiers, indicating a direct mechanical cost (Gursky, 2003,
2007; Schradin & Anzenberger, 2001). Additionally, detailed estimates
of locomotor cost in yellow baboons suggest that that the energetic
costs of infant transport may strongly determine the age of locomotor
independence (Figure 1; Altmann & Samuels 1992). Nevertheless, the
relationship between infant carrying and maternal locomotor energetics
is not always straightforward. Pontzer and Wrangham (2006) found
that the presence of a carried infant had no effect on chimpanzee
female daily travel distances, suggesting that mothers may have mecha-
nisms of compensating for the increased cost of carrying the infant’s
mass, perhaps through increased foraging. Rather, traveling with an
independent juvenile significantly decreased daily travel distances for
chimpanzee mothers, suggesting that needing to keep pace with an
inefficient offspring can also be costly. Again, it may be that the larger
size, and relatively reduced metabolic rate, of chimpanzees, buffers
them from energetic concerns that may plague smaller primates.
In general, across primates we expected that after adjusting for the
effects of adult female body mass, age at locomotor independence
would be negatively correlated with neonatal body mass and postnatal
growth rate, such that species with relatively large, fast-growing infants
would achieve locomotor independence at earlier ages. Instead, regres-
sion analyses showed that after controlling for body size differences,
neither neonatal mass nor postnatal growth rate were significantly
associated with age at locomotor independence (Table 3). In fact, age
at locomotor independence was nearly significantly (p 5 0.08) positively
associated with neonatal body mass, in direct opposition to our predic-
tions. Six of the prosimians in our primate sample park their infants,
rather than transport them (i.e., Microcebus rufus, Varecia variegata, Gal-
ago senegalensis, Otolemur crassicaudatus, Perodicticus potto, and Tarsier
tarsier). Because parking has been proposed to be a strategy for limiting
the energetic cost of infant carrying (Gursky, 2003, 2007; Ross, 2001;
46 | YOUNG ET AL.

FIGURE 5 Partial-regression plots (Quinn & Keough, 2002) of age at locomotor independence versus endocranial volume (a) and total age
at locomotor independence (i.e., the sum of postnatal age at independence and gestation length; Garwicz et al., 2009) versus endocranial
volume (b). Trend lines indicate the independent association between the two variables, controlling for the effects of adult female body
mass and phylogeny using multiple PGLS. Note that due to collinearity between body mass and endocranial volume, statistically this
relationship was analyzed using ridge regression of phylogenetic independent contrasts (see text for details). However, we use PGLS
derived partial-regression plots to more intuitively represent the relationship between locomotor independence and endocranial volume.
Due to high phylogenetic signal for these variables (see Table 2), PGLS derived relationships were very similar to results using independent
contrasts

but see Tecot, Baden, Romine, & Kamilar, 2012b), one might expect a
stronger link between infant size and locomotor independence in spe-
cies that continuously transport infants. However, analyses of the sub-
set of species that continuously transport infants also failed to show a
significant association between age at locomotor independence and
either neonatal mass (p 5 0.508) or postnatal growth rate (p 5 0.642).
2.6 | Influence of brain size
Independent locomotion is predicated on sufficient development of the
motor control system, including outgrowth of relevant spinal tracts
representing 11 orders.1 Moreover, the tight association between brain
size and age at walking onset remained after adjusting for the effects
of body size via partial correlation. These data support the premise that
motor development proceeds relatively slowly in more encephalized
species.
Garwicz et al. (2009) included four primates in their comparative
sample (Macaca mulatta, Pan troglodytes, Gorilla gorilla, and Homo sapi-
ens). To test whether a similar linkage between brain size and the pace
of motor development holds across primates, we used ridge regression
of phylogenetic independent contrasts to test for associations between
endocranial volume (an isometric proxy of brain size in primates: Isler

from the central nervous system, the pruning and refinement of effec- et al., 2008) and age at locomotor independence, controlling for the

tor neurons in the peripheral nervous system, and the maturation of influence of adult female body mass. We found that, independent of

higher level control centers, such as the cerebellum (Eyre, Taylor, Vil-
lagra, Smith, & Miller, 2001; Kolb & Whishaw, 1996; Kuypers, 1962;
Paus et al., 1999; ten Donkalaar, 2000). Because the rate of brain
development is similar across mammals (Passingham, 1985), species
with larger brains should exhibit protracted durations of behavioral
development, as growing infants wait for relevant neural substrates to
sufficiently mature. Moreover, growing a large brain is energeticially
expensive, and may come at the cost of slower somatic development,
including slower development of the musculoskeletal substrates
required for mature locomotion (but see Barrickman & Lin, 2010;
Deaner, Barton, & van Schaik, 2003). In a recent comparative study,
Garwicz, Christensson, and Psouni (2009) found that absolute brain
size was the best predictor of age at walking onset across 24 mammals
body size, endocranial volume was highly correlated with age at loco-
motor independence, whether locomotor independence is timed rela-
tive to birth (Table 3, Figure 5a) or relative to conception (as in Garwicz
et al. 2009; Figure 5b). Species with relatively late ages of locomotor
independence for their body size (i.e., Lagothrix poeppigii and hominids)
now follow the general primate trend when plotted against residual
1
Garwicz et al. (2009) coded walking onset as the earliest spontaneous use
of regular gait, which would occur at earlier ages than locomotor independ-
ence, as defined in the current study. Also, in order to account for prenatal
brain development—particularly in precocial mammals, such as ungulates—
Garwicz et al. (2009) calculated the age of walking onset from the concep-
tion, rather than birth (i.e., postnatal age of walking onset plus gestation
length).
YOUNG ET AL. | 47

endocranial volume, suggesting that relatively large brain size might

explain these species’ protracted motor development.
In summary, more encephalized primates achieve locomotor inde-
pendence at relatively late ages, even after adjusting for the effects of
body mass. In fact, greater encephalization is associated with pro-
tracted developmental periods, and a longer lifespan overall, across pri-
mates (Barrickman et al., 2008). Ridge regressions also showed that,
when controlling for endocranial volume, residual age at locomotor
independence was negatively associated with adult female body mass
(Table 3). In other words, if two differently sized primate species exhibit
similar brain sizes, the larger (i.e., less encephalized) species will become
independent at a relatively earlier age than the smaller one. In their
more expanded study of mammals, Garwicz et al. (2009) observed a
similar negative relationship between body size and age at walking
onset after controlling for absolute brain size (though the association
was not significant, at p 5 0.13).

FIGURE 6 Effects of arboreality/terrestriality on age locomotor

2.7 | Ecological influences
independence, adjusting for female body mass and phylogenetic
If the timing of locomotor development is at least partially determined relatedness using PGLS analysis of covariance. Symbols for primate
families follow Figures 3, 4 and 5
by the energetic cost to the mother and the developing infant, age at
locomotor independence should be correlated with daily travel distance
exploratory attempts at independent locomotion. Though no infants
(Altmann & Samuels, 1992; Pontzer & Wrangham, 2006). Specifically,
were injured due to falling, either the infant or a caregiver had to
we predicted that after controlling for variation in body size, age at
expend the energy to descend to the forest floor and climb back to a
locomotor independence would be negatively correlated with daily
€rster and Cords (2002) observed
safe arboreal location. Similarly, Fo
path length, such that species characterized by greater ranging costs
infant blue monkeys (Cercopithecus mitis) occasionally falling from
will achieve locomotor independence at earlier ages. However, PGLS
perches during the first 4 months of life. Though none of the infants
regression indicated that mass-specific daily path lengths were not
appeared to be injured, either they or a caregiver had to expend the
associated with age at locomotor independence (Table 3). This lack of
energy and time to climb back up to an arboreal location. Overall, we
association between daily path length and age at locomotor independ-
expected that to minimize risk of injury and energetic cost of falling,
ence may reflect a balance between the costs and benefits of extend-
selection for early locomotor independence should be tempered in the
ing ranging. Pontzer and Kamilar (2008) showed that across mammals,
more arboreal taxa. However, a phylogenetic ANCOVA in which modal
longer daily path lengths were associated with greater fertility, even
substrate (arboreal or terrestrial) was entered as a categorical factor
after controlling for the influence of body mass on these measures.
and adult female body mass as the covariate, showed that substrate
These data suggest that greater ranging may beneficially supplement
preference was not significantly related to age at locomotor independ-
access to foraging resources, negating the energetic cost of increased
ence (Table 3). In fact, the PGLS trend lines for arboreal and terrestrial
travel. A similar argument could apply to the accrued cost of infant car-
taxa were nearly superimposed on one another (Figure 6). Therefore,
rying during travel, where longer daily path lengths increase resource
though danger from falling may be an influential selective force in
uptake and offset any additional costs to the caretaker.
some species (Gursky, 2007; Morland, 1990), modal substrate usage
We also predicted that species characterized by a greater degree
does not have a significant effect on the age at which primates overall
of terrestrial travel would achieve locomotor independence at earlier
reach locomotor independence.
ages than more exclusively arboreal species. The arboreal habitat is dis-
continuous, multidimensional, and frequently unstable. Developing
2.8 | Discussion
arboreal infants therefore face a host of locomotor challenges not
encountered when moving terrestrially—as attested by the frequency Though the age of locomotor independence is quite variable across pri-
of long bone traumas due to falling in free-ranging primates (Bramblett, mates (Table 1), our analyses indicated some clear evolutionary corre-
1967; Buikstra, 1975; Carter, Pontzer, Wrangham, & Peterhans, 2008; lates of this variation. First, age at locomotor independence is
Jurmain, 1997; Lovell, 1991; Schultz, 1944). Studies of locomotor phylogenetically conserved, such that various primate clades display
development corroborate these dangers. Morland (1990) found that similar patterns of locomotor independence. For instance, cercopithe-
falling from nesting and parking sites was the most common cause of cids tend to become independent at relatively young ages, whereas
infant mortality in ruffed lemurs (Varecia variegata). Gursky (2007) hominids show independence relatively late (Figure 3b). Second, like
noted that young spectral tarsier infants often fall, initially from loca- many life history variables (Harvey & Clutton-Brock, 1985), age at loco-
tions where they have been parked, and at later ages during initial motor independence is positively associated with adult female body
48 | YOUNG
mass. Third, age at locomotor independence is correlated with age at
weaning (Figure 4). As noted above, such a correlation between nutri-
tional and locomotor independence should be expected on ecological
grounds. A juvenile that must secure its own foraging resources, per-
haps in direct competition with adult group mates (Janson & van
Schaik, 1993), should have sufficient locomotor abilities to access such
resources. Finally, age at locomotor independence is highly correlated
with brain size, even after adjusting for the effects of body size on
these variables. Taxa shown to be divergent when plotted relative to
other measures (e.g., Lagothrix and nonhuman hominids) instead follow
the common primate trend when plotted against residual endocranial
volume (Figure 5). Brain size has been shown to be a significant predic-
tor of life history variation across primates (Barrickman et al., 2008;
Deaner et al., 2003; Godfrey, Samonds, Jungers, & Sutherland, 2001;
Harvey & Clutton-Brock, 1985; Harvey et al., 1987; Isler & Van Schaik,
2012; Leigh, 2004; Leigh & Blomquist, 2007; Pereira & Leigh, 2003;
Ross & Jones, 1999; van Schaik & Deaner, 2003). Primates with large
brains generally take longer to reach maturity, as reflected by longer
gestation periods, longer periods of adolescence, later ages at first
reproduction, and—as shown here—later ages of locomotor independ-
ence. These “developmental costs of encephalization,” to borrow a
phrase from Barrickman et al. (2008), are balanced by the benefit of
having a longer reproductive adulthood (i.e., lifespan after age at first
reproduction).
There are two nonmutually exclusive reasons to suspect that larger-
brained primates would also have delayed ages of locomotor independ-
ence. The first arises from the energetic burden of growing a large brain.
Brains are metabolically expensive organs (Aiello & Wheeler, 1995), and
energy that is shunted towards brain development or maintenance can-
not be used for somatic growth (Sacher & Staffeldt, 1974; Wood, 2003).
Thus, extended developmental periods in more encephalized primates
are necessary to marshal sufficient resources for brain development
without risking stunted somatic growth, or worse, starvation (Deaner
et al., 2003). Second, functional neural development (e.g., myelination)
proceeds at a slower rate in species with larger brains (Gibson, 1991). In
summary, both the neural substrates required to direct locomotor
behavior and the somatic musculoskeletal structures needed to effectu-
ate that behavior develop more slowly in more encephalized animals,
likely leading to later ages at locomotor independence.
Our analyses were not exhaustive. Other ecological and behavioral
factors could, and should, be considered in future analyses of the
determinants wild primate locomotor development. Specifically, diet,
degree of allocare (i.e., infant transport and provisioning by multiple
individuals), degree of predation risk, and even social structure, could
all potentially influence the pace of locomotor independence. However,
initial pilot analyses with some variables of these variables did not sug-
gest a significant relationship with age at locomotor independence: nei-
ther diet (coded as percent of leaves in the diet, from Kamilar &
Cooper, 2013) nor the presence of allocare (coded as a binary variable
using data from: Ross, 2003; Tecot et al., 2012a) were significantly
associated with variation in ages at locomotor independence. Never-
theless, future analyses—perhaps using a taxonomically expanded data-
set—should consider these influences. Additionally, as discussed above,
ET AL.
milestones of behavioral maturity—such as weaning and locomotor
independence—are rarely binary phenomena, but represent the final
outcome of variable, asymptotic processes (Adolph, Robinson, Young,
& Gill-Alvarez, 2008). Only detailed, longitudinal studies of wild primate
infant development can parse the dynamic interplay between locomo-
tor independence, nutritional independence, and the myriad other eco-
logical challenges faced by growing primates.
3 | FUNCTIONAL ASPECTS OF PRIMATE
MUSCULOSKELETAL GROWTH
Once independent, juvenile primates must often operate within similar
ecological niches as adult conspecifics, competing for the same resour-
ces and evading the same predators. Nevertheless, smaller body size,
reduced muscle mass, lack of complete sensory-motor integration, and
general musculoskeletal immaturity may endanger juveniles through
increased predation risk and intraspecific resource competition with
more competent adults (Carrier, 1996; Herrel & Gibb, 2006; Janson &
van Schaik, 1993; Werner & Gillam, 1984; Wunderlich, Lawler, & Wil-
liams, 2011). Because, by definition, juveniles have yet to reproduce,
we should expect strong selection for mechanisms that could poten-
tially offset ontogenetic limits on performance, allowing individuals to
reach the adult stage of life, reproduce, and maintain or increase fitness
(Carrier, 1996; Herrel & Gibb, 2006; Husak, 2006; Irschick, Meyers, &
Husak, 2008; Jayne & Bennett, 1990; Le Galliard, Clobert, & Ferrière,
2004; Miles, 2004). Here we review several examples of how specific
ontogenetic allometries during primate growth may enhance the loco-
motor performance and safety of young primates, perhaps compensat-
ing for some of the inherent limitations of somatic immaturity.
3.1 | Body size
The small body size of juveniles can be a liability, as smaller individuals
typically suffer the bulk of predation pressure in ecological commun-
ities (Sinclair, Mduma, & Brashares, 2003). However, in some instances,
small body size can also provide beneficial opportunities to juveniles,
permitting them to access regions of the habitat not available to larger
adult group mates (Bezanson & Morbeck, 2013; Bezanson, 2017). For
instance, field studies of primate locomotor ontogeny have found that
the smaller body size of infants and juveniles allows them to engage in
more acrobatic arboreal locomotion and move on smaller substrates
than adults (Bezanson, 2006, 2009; Doran, 1992, 1997; Dunbar &
Badam, 1998; Dunham, 2015; Fan, Scott, Fei, & Ma, 2012; Sarringhaus,
MacLatchy, & Mitani, 2014; Sugardjito & van Hooff, 1986; Wells &
Turnquist, 2001; Workman & Covert, 2005; Wright, 2005; Zhu, Garber,
Bezanson, Qi, & Li, 2014). These observations illustrate the importance
of body size in determining the “locomotor niche” available to an ani-
mal, particularly when arboreal (Fleagle & Mittermeier, 1980; Jenkins,
1974). The differentiation of locomotor behavior and niche space
according to size and age class may allay the pressure juveniles would
otherwise face if forced to competitively forage against larger and
more experienced adults. However, other selective pressures, such as
predation, may force juveniles into more compromising spatial locations
YOUNG ET AL.
within the group structure. This could be particularly true during forag-
ing, when vigilance levels may be lower due to concentration on locat-
ing and processing food. For example, juvenile brown capuchins
(Sapajus apella) are known to maintain positions near the group center
when foraging. Although this intensifies feeding competition, it may
minimize predation pressure (Janson, 1990; Janson & van Schaik,
1993; but see O’Mara, 2015; Stone, 2006; Stone, 2007a, 2007b).
3.2 | Mechanical advantage
Limbs typically operate as levers, powered by muscular torque applied
at varying distances from the joint (Gray, 1944). The ratio of the length
of the lever arm of the limb muscles (usually abbreviated as “r”) to the
length of the load arm of the forces that the limb muscles must oppose
(typically abbreviated as “R”) is known as the “effective mechanical
advantage” of the limb muscles at the joint (i.e., EMA: Biewener, 2003)
(Figure 7). Effective mechanical advantage can be thought of as the
leverage of the joint - increasing mechanical advantage reduces the
muscular force required to produce a given output force. Similarly,
increasing mechanical advantage will increase levels of output force for
a given level of muscle force.
FIGURE 7 Static determinants of mechanical advantage at a limb
joint. Due to torque balance about the joint, the magnitude of the
output force (Fs) produced for a given muscle force (Fm) is
proportional to the ratio of the muscle’s lever arm length (r) and
the load arm length of the substrate reaction force (R). The ratio of
r and R (i.e., r/R) defines the effective mechanical advantage (EMA)
of the limb joint at this particular instance in the gait cycle. Note
that R can be altered either via morphological changes in limb
length or behavioral changes in limb posture. R0 indicates skeletal
limb length distal the joint in question, the proxy load arm length
used to calculate anatomical mechanical advantage (i.e., AMA).
Figure modified from Young (2005)
| 49
Biomechanically, muscle lever arm lengths can be reasonably
approximated with accurate measurements of musculoskeletal geome-
try (Biewener, Farley, Roberts, & Temaner, 2004). The load arm of the
ground reaction force, however, can only be estimated using a combi-
nation of kinematic data on limb posture and kinetic data on the direc-
tion and point of application of the substrate reaction force (Biewener,
1989, 1991). Given that accurate, high-resolution kinematic and kinetic
data are typically only available in a laboratory setting, effective
mechanical advantage has only been measured in a small sample of ani-
mals (Biewener, 1989; Biewener et al., 2004; Blob & Biewener, 2001;
Carrier, Gregersen, & Silverton, 1998; Polk, 2002; Smith & Wilson,
2013). Nevertheless, EMA can be reasonably approximated by calculat-
ing “anatomical mechanical advantage” (AMA), equal to the quotient of
bony muscle lever arm length and skeletal limb length distal to the joint
(Figure 7) (Bergmann & Hare-Drubka, 2015; Carrier, 1983; Fellmann,
2012; Smith & Savage, 1956; Young, 2005; Young, Danczak, Russo, &
Fellmann, 2014). Though variation in distal limb length is not always
perfectly correlated with substrate reaction force load arm length
(Young, 2009), AMA is a useful proxy when comparing the capacity for
force development across taxa (Bergmann & Hare-Drubka, 2015; Hil-
debrand & Goslow, 2001; Smith & Savage, 1956).
Very few studies have documented ontogenetic changes in
mechanical advantage. Greater mechanical advantage at young ages
would decrease the amount of muscle force required to maintain pos-
ture or effect movement, perhaps permitting increased performance in
juvenile animals despite musculoskeletal immaturity. If this were the
case, one would expect mechanical advantage to decline with size dur-
ing growth, the opposite of the trend observed with interspecific
increases in size across adult mammals, where larger animals typically
have greater EMA (Biewener, 1989; Polk, 2004; but see Day & Jayne,
2007; Reilly, McElroy, & Biknevicius, 2007). Carrier (1983) found that
AMA at several limb joints significantly decreases during growth in
both jackrabbits (Lepus californicus) and domestic cats (Felis catus). Cot-
tontail rabbits (Sylvilagus floridanus) are also characterized by declining
AMA during growth (J. W. Young and C. Fellmann, unpublished data).
With regard to primates, Young (2005) found that estimates of triceps
brachii and biceps brachii AMA at the elbow significantly decreased
over the first 4.5 years of life in capuchin monkeys (i.e., Cebus albifrons
and Sapajus apella; Figure 8). High AMA, relative to adult values, has
also been documented for the hip musculature (i.e., iliopsoas, gluteus
minimus, and gluteus medius) of immature macaques (Macaca fasicularis,
M. fuscata and M. mulatta) and yellow baboons (Papio cynocephalus)
(Fellmann, 2011). Evidence of similar ontogenetic trends across this
broad taxonomic sample, from jackrabbits, to cats, to primates, sup-
ports Carrier’s (1983:35) contention that “a loss of mechanical advant-
age may be the general condition for mammalian cursors and possibly
all mammals”. However, it should be noted that Fellmann (2011, 2012)
found that AMA for other limb muscles (i.e., biceps brachii at the elbow
and quadriceps femoris at the knee) tended to either remain static or
increase during development in a broad sample of catarrhine primates.
Therefore, universal ontogenetic decreases in AMA cannot necessarily
be assumed. Overall, more ontogenetic studies of developmental
50 | YOUNG
FIGURE 8 Ontogenetic changes in triceps brachii anatomical
mechanical advantage (AMA) in two species of capuchin monkey
(Cebus albifrons and Sapajus apella). Trends lines represent LOESS
fits to the data for each species. The vertical dashed line indicates
the age of locomotor independence in S. apella (Escobar-P
aramo,
1989; Table 1). Data on age at locomotor independence were
unavailable for C. albifrons, but ontogenetic studies of other
species of capuchin monkeys (i.e., C. capucinus and C. olivaceus)
suggest that independence for this should be roughly
contemporaneous. Note that triceps brachii AMA significantly
declines during the first 4.5 years of life, with most of the decrease
taking place after locomotor independence has been achieved.
Similar trends were documented for biceps brachii AMA as well
(Young, 2005)
changes in joint mechanics are required before common trends can be
discerned.
3.3 | Bone strength
Previous ontogenetic studies of a diverse array of mammals and birds,
including rats, chinchillas, domestic rabbits, hares, goats, muskoxen, and
gulls have also found that limb bone cross-sectional dimensions (i.e.,
external diameters and moments of area) scale with negative allometry
during growth (Carrier, 1983; Carrier & Leon, 1990; Heinrich, Ruff, &
Adamczewski, 1999; Lammers & German, 2002; Main & Biewener,
2004). Negative ontogenetic allometry of cross-sectional dimensions
indicate that young mammals have more robust bones (i.e., their bones
are structurally strong relative to their size), potentially compensating
for the incomplete mineralization, lower elastic modulus and greater
malleability of young mammalian bone by geometrically increasing
bone strength (Brear, Currey, & Pond, 1990; Carrier, 1983; Currey,
1984, 2001; Heinrich et al., 1999; Main & Biewener, 2004, 2007; Tor-
zilli, Takebe, Burnstein, & Heiple, 1981). Greater robusticity and
increased malleability combine to make young bones much tougher
than adult bones (i.e., young bones absorb more strain energy prior to
fracture: Currey, 2001, 2002; Currey & Butler, 1975). Increased bone
strength may permit young animals to exhibit near-maximal levels of
ET AL.
locomotor performance with reduced risk of skeletal injury (Main &
Biewener, 2004, 2006, 2007).
A priori, it could be assumed that primates might not follow this
general trend of relatively greater bone strength at young ages. As
reviewed above, primates are secondarily altricial at birth—infants pos-
sess well-developed sensory systems but are nevertheless strongly
dependent on their parents for subsistence and transport (Portmann,
1958). Previous research has primarily focused on precocial taxa—such
as goats—in which neonates are morphologically well-developed and
able to independently locomote soon after birth (Starck & Ricklefs,
1998). Altricial species, such as primates, have received relatively little
attention. Due to extended parental care and early immobility, altricial
species may be sheltered from the selective pressures thought to influ-
ence bone growth in very young precocial mammals. Indeed, Young,
Fern
andez, and Fleagle (2010) found that the mid-diaphyseal polar sec-
tion modulus (i.e., ZP, a structural measure of overall bending strength)
of the humerus and femur generally scales to body mass with isometry
in capuchin monkeys (Cebus albifrons and Sapajus apella) (Figure 9a,b).
Isometric scaling suggests that bone robusticity is maintained during
growth, and that young capuchin monkeys do not exhibit greater bone
robusticity, as commonly seen in precocial mammals. However, bone
lengths scale to body mass with strong positive allometry across limbs
and species, indicating that young capuchin monkeys are relatively
short-limbed for their size (Figure 9c,d; see also Jungers & Fleagle,
1980). Indeed, positive ontogenetic allometry of long bone lengths is
the modal pattern across primates and other altricial animals (Young,
2009). Because bending loads are proportional to both force magnitude
and bone length, developmental changes in limb length should be
incorporated into assessments of bone strength (Alexander, 1983; Ruff,
2000, 2003; Young et al., 2014). Indeed, when humeral and femoral ZP
are scaled to the product of body mass and bone length, a biomechani-
cally more appropriate size variable, negative allometry is the most
common pattern in both species (Figure 9e,f). Only the C. albifrons
femur, which scales isometrically, differs from the predominant pattern
of negative allometry. In summary, when biomechanically appropriate
size variables are used, long bone cross-sectional dimensions generally
grow with negative allometry in altricial capuchin monkeys, matching
the scaling patterns observed in previous ontogenetic studies of more
precocial animals (e.g., Carrier, 1983; Heinrich et al., 1999; Lammers &
German, 2002; Main & Biewener, 2004, 2007). Ruff (2003) found that
similar ontogenetic decreases in humeral and femoral bone robusticity
also characterize growing baboons (Papio cynocephalus) and humans
(Homo sapiens).
Previous studies have also found that ontogenetic changes in rela-
tive bone strength can parallel concomitant developmental changes in
locomotor behaviors. For example, Russo and Young (2011) found that
tail bone robusticity scales with negative allometry in capuchin mon-
keys, tracking a developmental decrease in the use of tail suspension
during feeding, foraging, and social behaviors (Bezanson, 2012; Mat-
thews, 2008). Along these lines, several studies have documented
ontogenetic changes in the relative strength of forelimb and hindlimb
bones that parallel developmental changes in forelimb and hindlimb
loading. For example, in humans, the relative robusticity of the femur
YOUNG ET AL. | 51

F I G U R E 9 Ontogenetic scaling of humeral and femoral dimensions in Cebus albifrons and Sapajus apella. Panels depict the scaling of
humeral and femoral polar section moduli (ZP, a geometric estimate of average bone strength in bending) on body mass (a and b), humeral
and femoral lengths on body mass (c and d), and humeral and femoral ZP on the product of body mass and bone length (e and f). Gray
symbols and dashed trend lines represent C. albifrons, black symbols and solid trend lines represent S. apella, and the dotted trend lines
indicate isometric scaling. Data from Young et al. (2009)

steadily increases from the first year of life through adulthood, with the
most dramatic increases taking place between the first and second
year, when most toddlers are becoming habitual bipedal walkers (Ruff,
2003). Similarly, in young mountain gorillas (Gorilla berengei) and com-
mon chimpanzees (Pan troglodytes), the relative strength of hindlimb
versus forelimb bones tracks developmental changes in arboreality ver-
sus terrestriality, with relative femoral strength dramatically increasing
as infants become increasingly adapted to terrestrial travel (Doran,
1997; Ruff, Burgess, Bromage, Mudakikwa, & McFarlin, 2013; Sarring-
haus et al., 2014; Sarringhaus, Maclatchy, & Mitani, 2016). Overall,
these studies suggest that, at least in some primates, there exists a
direct functional link between bone growth and the ontogenetic
changes in bone loading environments that take place during locomotor
development.
3.4 | Grasping morphology
Previous studies of primate growth have shown that infants and juve-
niles are characterized by relatively large hands and feet for their body
size (Druelle, Young, & Berillon, 2018; Ford & Corruccini, 1985; Grand,
52 | YOUNG
1977; Jungers, 1985; Jungers & Fleagle, 1980; Lawler, 2006; Lumer &
Schultz, 1947; Raichlen, 2005b; Ravosa, Meyers, & Glander, 1993;
Turner, Anapol, & Jolly, 1997; Turnquist & Wells, 1994). Relatively
large extremities with long digits have been argued to be functionally
adaptive for growing primates, permitting a more secure grasp of either
caregivers or arboreal substrates, as well as providing a larger, more
stable base of support (Jungers & Fleagle, 1980; Lawler, 2006; Wun-
derlich, Lawler, & Williams, 2011). Lawler (2006) presented quantitative
evidence on wild sifaka (Propithecus verreauxi) growth, locomotor devel-
opment, and life history supporting the assertion that relatively large
extremities may be evolutionary adaptive for juvenile animals. First,
Lawler (2006) found that, as in most primates, hand and foot lengths
scale to body mass with negative allometry during growth, indicating
that younger sifakas have relatively large extremities. Second, posi-
tional behavior data showed that juvenile sifakas frequently moved on
“adult-sized” substrates, rather than actively choose smaller substrates
that might have been easier to grasp, suggesting an ecological function
for relatively large hands and feet. Finally, combining morphometric
data with demographic data on life history, Lawler (2006) showed a
direct, positive relationship between foot length and survivorship to
reproductive maturity, strongly suggesting that relatively large extrem-
ities during the juvenile period are adaptively associated with increased
fitness in sifakas.
However, relatively large hands and feet are characteristic of many
infant and juvenile mammals, rather than being a uniquely primate trait
(Carrier, 1983; Lammers & German, 2002; Schilling & Petrovitch, 2006;
Young, 2009). Though there is little doubt that large hands and feet
could be beneficial during early locomotor efforts, particularly in arbo-
real species, the wide phylogenetic distribution of this growth pattern
potentially indicates that it is an epiphenomenon of general limb
growth dynamics, rather than indicative of selection for grasping per se.
Recently, Young and Heard-Booth (2016) and Druelle et al. (2018)
tested the hypothesis that the relatively large extremities of young pri-
mates are specifically associated with improved grasping ability by
examining the ontogeny of intrinsic digit proportions in capuchin mon-
keys (Cebus albifrons and Sapajus apella) and olive baboons (Papio anu-
bis). Previous studies have shown that intrinsic hand and foot
proportions (i.e., the lengths of the free digits relative to the metapo-
dials) are associated with increased grasping performance across tetra-
pods (Hamrick, 2001; Hopson, 2001; Kirk, Lemelin, Hamrick, Boyer, &
Bloch, 2008; Lemelin, 1995, 1999; Lemelin & Schmitt, 2007; Napier,
1961; Patel, Susman, Rossie, & Hill, 2009; Sustaita et al., 2013). Rela-
tively long digits increase grasping span, facilitating greater opposition
when wrapping the hand or foot around supports (but not necessarily
greater grasping precision: Lemelin & Grafton, 1998). Intrinsic digit pro-
portions are usually quantified by calculating phalangeal indices, equal
to the sum of proximal and intermediate phalanx lengths, divided by
the length of the corresponding metapodial (for the first rays, only
proximal phalanges are included in the numerator). In both capuchin
monkeys and olive baboons, phalangeal indices significantly decrease
over development, due to metapodial growth outpacing phalangeal
growth (Druelle et al., in press; Young & Heard-Booth, 2016). The rate
of decline is typically greater for pedal digits than for manual digits,
ET AL.
perhaps correlating with the greater importance of pedal grasping dur-
ing primate arboreal locomotion (Chadwell & Young, 2015; Cartmill,
1985; Gebo, 1993; Patel et al., 2015; Szalay & Dagosto, 1988). More-
over, in baboons, declining pedal phalangeal indices are directly associ-
ated with developmental decreases in the degree to which infants and
juveniles engage in hindlimb suspensory behaviors (Druelle et al., in
press). Finally, Patel, Organ, Jashashvili, Bui, & Dunsworth (2017)
recently showed in rhesus macaques (Macaca mulatta) and chimpan-
zees (Pan troglodytes), the bending robusticity of the first metatarsal is
greatest in infants prior to locomotor independence, suggesting that
immature primates are not only characterized by relatively long digits,
but relatively strong ones as well.
Overall, these findings are consistent with the hypothesis that pri-
mates are under selection for increased grasping ability early in life. Rel-
atively long and robust digits may be functionally adaptive for infant
and juvenile primates, permitting a more secure grasp on both caregiv-
ers and arboreal supports, as well as facilitating a wider array of posi-
tional behaviors during early foraging or social activities (such as play).
Nevertheless, additional studies of primates and other mammals, com-
bined with data on ontogenetic changes in grasping performance, are
required to fully evaluate the adaptive significance of primate hand and
foot growth.
4 | PRIMATE LOCOMOTOR DEVELOPMENT
AS A MODEL SYSTEM
Infants are not miniature adults; their body size and shape change dra-
matically during the growth period, and these developmental changes
affect locomotor performance (Adolph, Vereijken, & Shrout, 2003; Car-
rier, 1983; Eilam, 1997; Grand, 1977; Jensen & Bothner, 1998; Jungers
& Fleagle, 1980; Lammers & German, 2002; Lumer & Schultz, 1941;
Main & Biewener, 2004; Muir, 2000; Pflieger, Cassidy, & Cabana,
1996; Raichlen, 2005a, 2005b; Ruff, 2003; Shapiro & Raichlen, 2006;
Shapiro & Young, 2012; Thelen, Fisher, & Ridley-Johnson, 1984;
Turnquist & Wells, 1994; Young, 2009, 2012a, 2012b; Young & Heard-
Booth, 2016). Therefore, longitudinal (or cross-sectional) intraspecific
studies of the ontogeny of the musculoskeletal system in relation to
locomotor performance permit a “real-time” test of form-function rela-
tionships, without the confounding effects of phylogeny that may com-
plicate adult interspecific studies (Barr, 2014; Hurov, 1991; Kamilar &
Cooper, 2013; Nunn, 2011; O’Neill & Dobson, 2008). Moreover, in
some cases the magnitudes of morphological and behavioral variation
during growth may be greater than interspecific levels of variation
among adult primates (see section on gait ontogeny below), permitting
a finer-scale exploration of form-function associations. Exploring the
relationship between morphological growth and locomotor ontogeny
therefore provides insight not only into selective pressures on young
animals (see above), but into the functional morphology and evolution
of adult locomotion. Below, we provide examples in which locomotor
ontogeny has been employed as a model system to understand the bio-
mechanics of primate quadrupedalism, arguably the most thoroughly
studied (nonhuman) primate locomotor behavior from both develop-
mental and adult perspectives.
YOUNG ET AL.
4.1 | Primate quadrupedalism
Ontogenetic studies have improved our understanding of some of the
relatively unique biomechanical features of primate quadrupedal loco-
motion that have been revealed by laboratory (and occasionally field)
based studies of adult primates. Unlike quadrupedal walking in most
other mammals, (adult) primate quadrupedalism is characterized by a
preference for diagonal sequence, diagonal couplets (DSDC) gait,
increased humeral protraction at touchdown, reduced vertical substrate
reaction forces on forelimbs relative to hindlimbs, joint yield during the
support phase, high duty factors, large limb excursion angles, long
strides, and low stride frequencies (Alexander & Maloiy, 1984; Demes
et al., 1994; Hildebrand, 1967; Kimura et al., 1979; Larson, Schmitt,
Lemelin, & Hamrick, 2000; Reynolds, 1985). These distinctive aspects
of primate quadrupedalism are often viewed as part of a functional
complex that facilitated the early evolution of primates in a “fine
branch niche” by providing stability on (relatively) narrow, flexible
branches. The kinematic features listed above enhance stability by
reducing branch oscillations and fluctuations of the body’s center of
mass, and by allowing primates to increase speed while maintaining
contact with the substrate (Cartmill, Lemelin, & Schmitt, 2002; Demes,
Jungers, & Nieschalk, 1990; Larson, 1998; Larson et al., 2000, 2001;
Lemelin, Schmitt, & Cartmill, 2003; Li, 2000; Prost & Sussman, 1969;
Rollinson & Martin, 1981; Schmitt, 1999; Schmitt, 2003a, 2003b;
Stevens, 2003; Vilensky, Moore, & Libii, 1994). Kinetically, the reduc-
tion of locomotor forces on the forelimbs compared to hindlimbs has
led to primates’ enhanced forelimb manipulatory abilities utilized for
navigation and foraging in a complex arboreal environment (Larson,
1998; Lemelin & Schmitt, 2007; Schmitt & Lemelin, 2002).
4.2 | Insights on primate quadrupedalism from
ontogeny
Notwithstanding the biomechanical/ecological hypotheses that have
been put forth to explain the evolution of the kinematic and kinetic
features of primate quadrupedal gait, ontogenetic analyses have con-
tributed novel insights on the proximate functional relationships
between morphology and gait biomechanics. Below we review exam-
ples of how ontogenetic studies have contributed toward our under-
standing of the distinctive aspects of primate quadrupedalism.
4.3 | Stride lengths and frequencies
As noted above, compared to other mammals, adult primates use rela-
tively long strides and low stride frequencies (Alexander & Maloiy,
1984). Raichlen (2005a, 2005b) used an ontogenetic sample of
baboons to test the hypothesis that the relatively long strides and low
stride frequencies characterizing adult primates could have evolved as
by-products of grasping extremities. Because musculature associated
with grasping is most accentuated in the distal aspects of the fore and
hindlimb, primates have relatively distally distributed limb mass com-
pared to non-grasping taxa. By increasing a limb’s natural pendular
period of oscillation, distally placed limb mass increases swing duration,
thus increasing overall stride duration and lowering stride frequency
| 53
€ nther, 1994; Raichlen, 2004).
(Myers & Steudel, 1997; Preuschoft & Gu
Since speed is the product of stride length and stride frequency, at a
given speed, low stride frequencies are associated with long strides.
An ontogenetic sample provides a natural experiment by which to
test this hypothesis. Because of their need to cling to their mother during
initial locomotor efforts, infant primates have more well developed grasp-
ing muscles and more distally distributed limb mass compared to adults
(Grand, 1977; Raichlen, 2005a; Turnquist & Wells, 1994). Accordingly, in
a longitudinal sample of baboons spanning the ages of 1–9 months, Rai-
chlen (2005a) found a proximal shift in limb mass distribution with age
^t, Moulin, & Berillon, 2017a). Young infants
(see also Druelle, Aerts, D’aou
with more distally distributed limb mass used relatively longer strides and
lower stride frequencies than older infants with more proximally distrib-
uted limb mass (Raichlen, 2005b). Thus, the ontogenetic shift in limb
mass distribution and quadrupedal kinematics paralleled the difference
between primates and other mammals, supporting the hypothesis of
grasping as a key component in the evolution of these stride characteris-
tics in primates. Raichlen also found at least partial support in the ontoge-
netic sample for the related hypothesis that grasping extremities, and
their associated distally distributed limb mass, may also be the proximate
explanation for primates’ elongated stance durations and large limb
excursions. That is, some, (but not all) of the younger infants with more
distally distributed limb masses had relatively longer stance durations and
step lengths than those with more proximally concentrated limb masses.
The explanation for these associations is that distally distributed limb
mass increases swing duration, stance duration increases in accordance
with swing duration, and increased stance duration increases step length,
necessitating broader limb excursion (Raichlen, 2005b).
Finally, the transition from distally to more proximally concentrated
limb mass in younger vs. older infant baboons (and its effect on stride
length and frequency) provided another opportunity to test a hypothe-
sis regarding the relationship between limb mass distribution and
energy cost (Raichlen, 2006). Although distally distributed limb mass
should theoretically increase energetic costs due to the increased rate
at which muscles must work to move the limb segments relative to the
body (internal power), counterintuitively, primates and other animals
with relatively distally distributed limb mass have not been shown to
have higher energetic costs than those with more proximally distrib-
uted limb mass (Heglund, 1985; Steudel-Numbers, 2003; Taylor,
Heglund, & Maloiy, 1982; Taylor, Shkolnik, Dmi’el, Baharav, & Borut,
1974). Raichlen’s (2006) alternative (“trade-off”) hypothesis considers
the contributions of both internal and external power, required to
move the limbs and the body’s center of mass, respectively. This
hypothesis states that distal limb mass distribution leads to lower stride
frequencies (lower internal power output) and longer strides (higher
external power output due to increased vertical displacement of the
body’s center of mass), such that total power remains comparable to
animals with proximal limb mass distribution. This hypothesis was par-
tially supported in the ontogenetic sample- in the youngest infant
baboons (when limb mass was most distally concentrated) lower stride
frequencies were associated with reduced internal power output, but
the relationship between longer strides and external power was less
clear (Raichlen, 2006).
54 | YOUNG
In sum, ontogenetic transitions in morphology and locomotor kine-
matics (at least among baboons) are consistent with the hypothesis
that at least some features of primate quadrupedalism can be explained
as an evolutionary by-product of grasping hands and feet. This
morphology-based view provides a more proximate explanation for the
evolution of primate kinematic features in a “small branch” ecological
setting, without the need to treat the kinematic features themselves as
heritable adaptations (Raichlen, 2005b).
4.4 | DSDC gait
The preference for DSDC gait in adult primates is not fully unique among
mammals, but is quite uncommon (Cartmill, Lemelin, & Schmitt, 2007a;
Hildebrand, 1967; Karantanis, Youlatos, & Rychlik, 2015; Lemelin et al.,
2003; Pridmore, 1994; Shapiro & Young, 2010; White, 1990). Compared
to lateral sequence (LS) gaits, DSDC gait appears to be associated with at
least two disadvantages—relatively small triangles of support during the
stride (which may not be relevant on narrow substrates such as branches),
and ipsilateral limb interference (Cartmill et al., 2007a; Rollinson & Martin,
1981). Arboreality, and specifically, the use of narrow, flexible branches is
common among some (but not all) of the few mammals that regularly use
DSDC gait (Hildebrand, 1967, 1976; Karantanis et al., 2015; Lemelin &
Cartmill, 2010; Lemelin et al., 2003; Pridmore, 1994; White, 1990).
Therefore, functional and adaptive explanations for DSDC gait have
focused on biomechanical stability, particularly in a precarious arboreal
setting. An arboreal explanation for DSDC gait usage is complicated by
the fact that some arboreal mammals that regularly navigate (or are capa-
ble of navigating) small, flexible branches do not prefer this gait (Karanta-
nis, Rychlik, Herrel, & Youlatos, 2017a, 2017b, 2017c; Schmidt & Fischer,
2010; Shapiro & Young, 2010, 2012; Shapiro, Young, & VandeBerg,
2014). Regardless, ontogeny has provided a means to test some of the
more proximate biomechanical hypotheses for why some mammals, and
primates in particular, prefer DSDC gaits. The utility of ontogeny for
understanding primate gait stems from the fact that 1) although adult pri-
mates show variability in gait types, the gait profile of infant and juvenile
primates is more variable than that of adults, and non-DS gaits (e.g., lat-
eral sequence, with either lateral or diagonal couplets; LSLC, LSDC) are
used much more frequently (Dunbar & Badam, 1998; Hildebrand, 1967;
Hurov, 1982; Nakano, 1996; Rollinson & Martin, 1981; Shapiro &
Raichlen, 2005, 2006; Vilensky & Gankiewicz, 1989; Young, 2012a), and
2) during growth, primates experience dramatic changes in body mass,
body mass distribution, and limb proportions (Druelle et al., 2017a;
Druelle et al., in press; Grand, 1977; Jungers & Fleagle, 1980; Leigh,
1992; Lumer & Schultz, 1941; Raichlen, 2005b; Shapiro & Raichlen,
2006; Turnquist & Wells, 1994; Young, 2005, 2009; Young & Heard-
Booth, 2016) permitting a direct real-time test of how such morphological
changes are correlated with gait selection.
4.5 | DSDC gait and limb placement
An important functional benefit of DSDC gait is that it maximizes peri-
ods of diagonally supporting fore- and hindlimbs, enhancing stability by
facilitating the production of opposing torques via grasping hands and
ET AL.
feet (Chadwell & Young, 2015; Cartmill et al., 2002; Preuschoft, 2002).
However, because this benefit stems not from the diagonal limb
sequence, but the diagonal limb couplets, it is not exclusive to DSDC
walking—it also characterizes LSDC walking (Cartmill et al., 2002). An
added advantage proposed for DSDC walking gait relates to the posi-
tioning of the limbs at a key moment of potential arboreal instability. In
DSDC gait, at the moment when a forelimb lands on a potentially
unstable substrate, the contralateral hindlimb should be positioned
under the body’s center of mass, potentially conferring stability (Cart-
mill et al., 2002; Shapiro & Raichlen, 2007b; Wallace & Demes, 2008) if
the subsequent support proves to be unstable. Determining whether
this advantage is exclusive to DSDC gait necessitates a comparison to
limb positioning in other gaits such as LSDC or LSLC, while also taking
into account that limb positioning is a combined result of interlimb tim-
ing, angular excursion of the limbs, and limb lengths relative to each
other and to trunk length (Hildebrand, 1980; Schmidt, 2008; Shapiro &
Raichlen, 2005, 2007b; Young, 2012a). Since primates use larger limb
excursions (Larson et al., 2001) than other animals that regularly use LS
gaits, it is best to compare limb positioning across gaits within primates
(Wallace & Demes, 2008). Ontogenetic studies can provide this oppor-
tunity, because infant primates use a wider variety of gaits than do
adults. For example, by comparing infant baboons that used either LS
or DS gaits, Shapiro and Raichlen (2005, 2007b) demonstrated that
both DSDC and LSLC walking ensure that a protracted hindlimb is posi-
tioned underneath the center of the body at the moment of forelimb
touchdown (see also Cartmill et al., 2007a). Moreover, the analysis
clarified that both gaits are accompanied by a hindlimb as well as a fore-
limb under the body. In DSDC, this (retracted) forelimb is ipsilateral to
the protracted hindlimb. In LSLC the (retracted) forelimb is contralateral
to the protracted hindlimb (Figure 10), with the potential to provide
additional stability from the opposing torques produced by contralat-
eral limb pairs (Hildebrand, 1980; Preuschoft, 2002).
Since adult primates do not use LSLC, it is unlikely that this type of
gait played a significant role in the evolution of primate quadrupedal-
ism. However, the use of ontogeny to test hypotheses about the bene-
fits of DSDC gait has proven to be fruitful and has helped highlight the
fact that DSDC does appear to be the only gait that combines both the
benefit of diagonal couplets (grasping torques generated by contralat-
eral limb pairs) and the benefit of limb positioning (placement of hind-
limb at moment of forelimb touchdown) (Cartmill Lemelin, & Schmitt,
2007b). A third benefit that has been identified for DSDC gait (tested
in a non-primate arboreal mammal, the kinkajou) is that it increases not
only the duration of support by diagonal limb pairs, but the linear dis-
tance between them, further enhancing stability (Lemelin & Cartmill,
2010). It is important to note that although the spatiotemporal features
of diagonal sequence, diagonal couplets gait are often presumed to
have evolved in response to relatively small-diameter substrates, they
are not strictly necessary for navigating small-diameter supports
(Karantanis et al., 2017a, 2017b, 2017c; Schmidt & Fischer, 2010;
Shapiro & Young, 2010, 2012; Shapiro et al., 2014), and changes in sub-
strate orientation or compliance tend to have a more significant effect
on gait parameters than substrate diameter per se (Shapiro & Young,
2010; Shapiro et al., 2014; Young, Stricklen, & Chadwell, 2016b).
YOUNG ET AL. | 55

FIGURE 10 Comparison of limb positioning at forelimb touchdown in infant baboons while walking in diagonal sequence, diagonal
couplets (DSDC; limb phase 70%, duty factor 62%), lateral sequence, lateral couplets (LSLC; limb phase 20%, duty factor 66%) and lateral
sequence, diagonal couplets (LSDC; limb phase 32%, duty factor 72%) gaits. Arrows indicate whether the limb is in support (down arrow) or
swing (up arrow). Note the increased potential for ipsilateral forelimb-hindlimb interference in DSDC compared to the LS gaits. Also,
forelimb-hindlimb pairs positioned beneath the center of the body are ipsilateral in DSDC, and contralateral in LSLC. In LSDC, there is
neither a supporting forelimb nor hindlimb beneath the center of the body. Each gait type is also represented with respect to the timing of
limb support (black bars) and swing phases (no bars) as a percentage of the total stride, with arrows indicating the moment in time captured
in the baboon images. R 5 Right, L 5 Left, F 5 Forelimb, H 5 Hindlimb. Limb phase is the percentage of a stride’s duration that the touch-
down of a forelimb follows that of the ipsilateral hindimb. Duty factor is the percentage of a stride that a limb is in contact with the
substrate. Images traced from video sequences (Shapiro & Raichlen, 2005)

4.6 | DSDC gait and the position of the body’s center
of mass
Previous researchers (Rollinson & Martin, 1981; Tomita, 1967) have
proposed that DSDC gaits are biomechanically more stable for primates
due to a presumably more caudal position of the body’s center of mass
1994; Vilensky, 1979; Wells & DeMenthon, 1987; Young, 2012a); 2)
experimental manipulations of body COM in primates, or comparisons
of primates with COM shifts due to tail fattening, do not result in pre-
dicted changes of footfall sequences (Young, Patel, & Stevens, 2007);
3) regardless of the position of the body’s center of mass, primates

compared to other animals. That is, when walking with diagonal cou- readily switch from DS to LS gaits under certain conditions (e.g., when

plets, if the body’s center of mass lies in front of a line connecting diag- moving from a narrow pole to the flat ground: Hesse, Nyakatura,

onal supporting limb pairs, the forelimb of the diagonal swinging limb Fischer, & Schmidt, 2015; Prost & Sussman, 1969; Shapiro, Young, &

pair should land first, encompassing the center of gravity vector within Souther, 2011; Stevens, 2006; Vilensky & Larson, 1989; Vilensky &

the supporting three limbs, preventing forward pitch, and resulting in
an LS gait (in which a forelimb lands before the contralateral hindlimb).
Alternatively, if the body’s center of mass lies behind the line connect-
ing the supporting diagonal limb pair (as it theoretically would be in a
primate with a caudally positioned center of mass), the hindlimb of the
diagonal swinging limb pair should land first, encompassing the center
of gravity vector within the supporting three limbs, preventing back-
ward pitch, and resulting in a DS gait. This explanation, known as the
“Support Polygon Model” (Cartmill et al., 2002, 2007a; Gray, 1944; Hil-
debrand, 1980; Tomita, 1967; Young, 2012a), is problematic for the fol-
lowing reasons: 1) the position of the whole body center of mass of
primates is not particularly caudal—in the few primate species in which
whole body COM has been measured, it appears to be located rela-
tively close to the craniocaudal midline (Crompton, Li, Alexander,
€ nther, 1996; Druelle et al., 2017a; Grand, 1983; Raichlen,
Wang, & Gu
Pontzer, Shapiro, & Sockol, 2009; Reynolds, 1974; Turnquist & Wells,
Patrick, 1985; Vilensky et al., 1994; Wallace & Demes, 2008) 4) in DS
gaits, the landing hindlimb of a diagonal pair is not necessarily in a posi-
tion to prevent backward pitch, and at that moment the direction of
pitch is likely forward anyway (Cartmill et al., 2007a); 5) the Support
Polygon Model is based on static stability, and primates most likely rely
more often on dynamic stability when travelling at any appreciable
speed (Chadwell & Young, 2015; Lammers & Zurcher, 2011; Larson &
Stern, 2006; Vilensky & Larson, 1989; Young et al., 2016b; Young,
Russo, Fellmann, Thatikunta, & Chadwell, 2015); and 6) the idea that
primates have a more caudal COM has been conflated with the hind-
limb “dominance” of primates compared to other mammals (i.e., higher
substrate reaction forces on hind compared to forelimbs). Yet limb
force distribution does not necessarily equate to center of mass posi-
tion; greater weight support on primate hindlimbs may stem from the
location of the body COM relative to the limbs, the kinematic position-
ing of the hands and feet relative to the COM (regardless of the latter’s
56 | YOUNG ET AL.

FIGURE 11 Ontogenetic variation in gait selection in Papio cynocephalus, Macaca fuscata, and Saimiri boliviensis during the first nine
postnatal months. Left hand panels display the frequencies of lateral sequence (LS) walking gaits (relative to all gaits). In all three species,
frequencies of lateral couplets (LSLC) increase as frequencies of diagonal couplets (LSDC) decrease (data compiled from: Nakano, 1996;
Shapiro & Raichlen, 2006; Young, 2012a). Right hand panels show the frequency of lateral sequence (LS) walking gaits (diagonal or lateral
couplets) relative to diagonal sequence, diagonal couplets (DSDC) walking gaits (data compiled from: Nakano, 1996; Shapiro & Raichlen,
2006; Young, 2012a)

fore-aft position), or an active shift to hindlimb weight support via mus-
cle recruitment (Raichlen et al., 2009; Reynolds, 1985; Young, 2012b).
Despite these concerns, some authors have cited primate gait selection
on oblique supports as evidence for a modified version of the Support
Polygon Model. Adult primates increase limb phase on inclines and
decrease limb phase on declines, leading to higher frequencies of DS
gaits on inclines and LS gaits on declines (Hesse et al., 2015; Nyakatura,
Fischer, & Schmidt, 2008; Nyakatura & Heymann, 2010; Prost & Suss-
man, 1969; Vilensky et al., 1994). Since moving on inclines projects the
gravity vector closer to the feet than through the midline and the
opposite is true for declines, there does appear to be a functional rela-
tionship between the position of the gravity vector and limb phase.
However, the gait patterns on inclines and declines are more function-
ally related to hindlimb propulsion against gravity and forelimb braking
against downward acceleration, than to limb footfalls to enclose sup-
port polygons (Birn-Jeffery & Higham, 2014; Hesse et al., 2015), and
what remains not well explained is why primates use DSDC gaits on
horizontal substrates.
Though a strict adherence to the Support Polygon Model has been
challenged in studies of adult primates, ontogenetic shifts both in the
YOUNG ET AL.
position of the whole-body COM and gait preferences provide another
means by which to test for a functional link between these two param-
eters. Although DSDC gait may be used frequently even at very early
ages (Hurov, 1982; Nakano, 1996; Shapiro & Raichlen, 2006; Young,
2012a), the type of LS gaits used by immature primates exhibit a shift
from LSDC to LSLC. This transition occurs at approximately 4–6
months in Papio (Shapiro & Raichlen, 2006) and Macaca (Hildebrand,
1967; Nakano, 1996), and after 6 months in Saimiri (Young, 2012a)
(Figure 11). As primates mature, their use of DS gaits become predomi-
nant (Figure 11). During growth, primates also experience dramatic
changes in body mass, body mass distribution, and limb proportions.
Within their first year, primates (at least, those for which we have
ontogenetic morphometric data - e.g. baboons, vervet monkeys, squir-
rel monkeys, macaques, chimpanzees), experience a caudal shift in the
whole body COM, brought about by a relative decrease in mass and
length of the head, combined with a relative increase in the length and
mass of the hindlimbs and the abdominal portion of the trunk (Bolter &
Zihlman, 2003; Druelle et al., 2017a; Grand, 1983; Turner et al., 1997;
Turnquist & Wells, 1994; Raichlen, 2005b; Schoonaert, D’aout, & Aerts,
2007; Shapiro & Raichlen, 2006; Vilensky, 1979; Young, 2012a). Thus,
the relatively cranial location of the COM in primate infants might be
functionally linked to their relatively frequent use of LS gaits, reinforc-
ing the Support Polygon Model. For example, growing Papio cynocepha-
lus experience an increase in frequency of DS relative to LS gaits
around the time when the whole-body COM moves caudal to the mid-
line of the trunk (Shapiro & Raichlen, 2006, 2007a). Druelle, Berillon,
and Aerts (2017b) also found a caudal movement of COM with
increase in use of DS for Papio anubis, but were hesitant to draw func-
tional links between COM position and gait preference, pointing
instead to the probable influence of neuromotor maturation. Young
(2012a) found that in an ontogenetic sample of infant and juvenile
squirrel monkeys, a caudal translation of the COM (from 47% to 58%
of trunk length) during growth increased the probability of using a DS
gait by 66% (on a flat surface) to 98% (on a pole). In that study, COM
position was determined to be a better predictor of gait choice than
either age or body mass, suggesting that body shape may be a more
critical factor for gait choice than general neuromotor maturation.
Thus, the influence of body shape on gait expressed in the ontogenetic
data appear to provide support for the Support Polygon Model, since
LS gaits are more frequent in infants who have relatively large heads,
less massive hindlimbs, and more cranially located whole body centers
of mass. However, as noted above, promotion of the Support Polygon
Model as a general explanation for adult primates’ use of DSDC gait is
complicated by several confounding factors, including the critical obser-
vation that adult COM appears to be close to the craniocaudal midline.
4.7 | DSDC gait and limb proportions
Gait selection in mammals is influenced by the need for stability, but
also by body shape. Variation among species in gait preferences is at
least partially influenced by variation in limb proportions, due to the
interaction between the timing of footfalls and the potential for ipsilat-
eral limb interference (Hildebrand, 1968, 1976, 1980). For example, the
| 57
potential for ipsilateral limb interference is very high in DSDC gaits.
Many primates avoid this complication by using a seemingly inefficient
gait pattern known as “overstriding”, where they pass the hindlimb
medial or lateral to the ispilateral forelimb when walking on the ground
(Cartmill et al., 2007a; Hildebrand, 1967; Larson & Stern, 1987) (Figure
10). The high potential for limb interference is considered to be one of
the main disadvantages of DSDC walking gait, and is exacerbated
when primates move on a narrow branch, where mediolateral over-
striding is not an option. Alternatively, ipsilateral limb interference can
be avoided by shortening hindlimb stride length, restricting retraction
of the forelimb, or limiting protraction of the hindlimb (Hildebrand,
1967; Schmidt, 2005, 2008; Young, 2012a). Conversely, because ipsi-
lateral limbs swing and land nearly simultaneously in LSLC walking or
simultaneously in the pace, there is little to no possibility of ipsilateral
limb interference associated with these gaits (i.e., the forelimb touches
down well forward of the hindlimb). Accordingly, LSLC and pacing are
preferred by mammals with elongated limbs (e.g., greyhound dogs and
camelids) (Hildebrand, 1968, 1976, 1980). LSDC gaits are intermediate
with respect to interference issues—the diagonal couplets lead to
increased spatial proximity of a swinging hindlimb to the supporting
ipsilateral forelimb, producing a higher potential for interference com-
pared to LSLC gaits or paces. However, due to the lateral footfall
sequence, the forelimb is typically lifted before the hindlimb touches
down, mitigating the potential for prolonged interference.
Because primates exhibit changes in both limb proportions and
gait frequencies during growth, ontogenetic analyses can be useful in
testing the link between gait type and limb interference potential. Most
primates exhibit an overall decrease in intermembral index during
ontogeny (Falsetti & Cole, 1992; Glander, 1994; Jungers & Fleagle,
1980; Ravosa et al., 1993; Schaefer & Nash, 2007; Shapiro & Raichlen,
2006; Shea, 1992; Turner et al., 1997; Turnquist & Wells, 1994; Wolf,
2011), such that the hindlimb elongates disproportionately relative to
the forelimb, though there are exceptions, particularly among homi-
noids (Buschang, 1982; Jungers & Cole, 1992; Jungers & Hartman,
1988; Ruff et al., 2013; Schoonaert et al., 2007; Shea, 1981). Combined
with the tendency for primates to use exaggerated hindlimb protraction
at touchdown (Larson et al., 2001), hindlimb elongation should lead to
increased potential for ipsilateral hind-fore interference. Thus, (because
of the interference problems associated with DSDC gait), one would
predict that the frequency of DSDC would decrease as relative hind-
limb length reaches a maximum (i.e., when the intermembral index is at
its minimum). This does not appear to be the case, however. For exam-
ple, in baboons, macaques, and squirrel monkeys, DSDC is frequently
used throughout the growth period, even when intermembral index
(IMI) is at its lowest value (Nakano, 1996; Shapiro & Raichlen, 2006;
Turnquist & Wells, 1994; Young, 2012a). On the other hand, one
would expect LSLC gait to increase in frequency as IMI decreases,
because of this gait’s benefits in avoidance of interference. Indeed,
there is some evidence supporting a functional link between intermem-
bral index and the couplets used during LS gait. In Papio cynocephalus,
for example, the time period during which the use of LSDC gaits was
replaced by LSLC gaits (5–6 months) (Figure 11) corresponded to the
time period in which IMI reached its lowest value (Figure 12) (Shapiro
58 | YOUNG
FIGURE 12 Variation in intermembral index (forelimb length as a
percentage of hindlimb length, excluding hands and feet) in Papio
cynocephalus, Macaca mulatta, and Saimiri boliviensis during the first
nine postnatal months (data compiled from: Shapiro & Raichlen,
2006; Turnquist & Wells, 1994; Young, 2008)
& Raichlen, 2006). The correlation of low IMI reduction and increased
LSLC also appears to be characteristic of macaque ontogeny, although
these two factors are only available in separate studies, for two differ-
ent species (Nakano, 1996; Turnquist & Wells, 1994) (Figures 11 & 12).
In infant and juvenile Saimiri, the potential for limb interference
(quantified with a measurement that took into account both limb
length and limb positioning), increased during growth. Increased poten-
tial for limb interference increased the probability of using LS gait by
57% (when moving on a pole), independent of the effects of body
COM position (Young, 2012a). Resembling ontogenetic gait trajectories
in LS gait reported for Papio and Macaca, there was a shift (within LS
gaits overall) from a preference for LSDC gaits at the youngest ages, to
the exclusive use of LSLC gaits after 6 months (Figure 11). Although
the shift did not correspond to a decrease in IMI (Figure 12) in this spe-
cies, the IMI of Saimiri was relatively low throughout the growth period.
These observations suggest the existence of a common mechanism
among growing primates to utilize gaits that help mitigate limb interfer-
ence. Increased potential for limb interference in Saimiri was shown to
have little effect on how frequently DSDC gait was used. However,
young squirrel monkeys were able to mitigate limb interference in DS
gaits (on a pole) by reducing forelimb retraction, even when hindlimb
protraction remained prominent (Young, 2012a). Thus, the use of kine-
matic adjustments even in the face of ontogenetic changes in limb pro-
portions provide insight on how adult primates may also mitigate the
interference disadvantage of DSDC, and may even provide an explana-
tion for the exaggerated forelimb protraction and hindlimb retraction
characterizing primates (Larson et al., 2001; Schmidt, 2005, 2008)
An important issue for ontogenetic analyses concerns the temporal
resolution at which data are collected, which can influence interpreta-
tions (Adolph et al., 2008). For example, in contrast to data reported
for Papio cynocephalus (Shapiro & Raichlen, 2006), Druelle et al.
ET AL.
(2017a) did not find a “dip” in the IMI of Papio anubis across the same
period of growth, although they pointed out that it “is likely to become
apparent with a shorter observation window.” That is, in the time frame
common to both studies (the first 9 months), Druelle et al. (2017a)
measured limb proportions every three months, compared to twice
each month in Shapiro and Raichlen (2006). Further study across more
species is needed to confirm the relationship between the ontogenetic
timing of gait preferences, IMI, and limb positioning (at least within LS
gaits). At present, while there are numerous studies reporting ontogeny
of IMI, fewer studies have documented gait preferences during the
growth period (data on strepsirrhines are particularly lacking).
4.8 | Ontogeny of limb postures
Another area where ontogenetic studies can serve as a model system,
or test case, relates to the effects of body mass on limb posture. It has
been shown across a broad interspecific mammalian sample (Biewener,
1989) as well as among cercopithecoid primates (Polk, 2002), that
larger animals use more extended limb postures (i.e. larger joint angles)
than smaller animals. Extended limb postures, by aligning limb seg-
ments more closely with the substrate reaction force vector, serve to
reduce bending forces on limb bones, and, by increasing effective
mechanical advantage, reduce the muscular force required to maintain
limb postures (Biewener, 1989; Polk, 2002). Extended limb postures
may also lower energetic costs during locomotion by increasing effec-
tive limb length (vertical distance from shoulder or hip to the ground:
Pontzer, 2007), and by increasing stride length, lead to faster speeds at
a given stride frequency. Although the use of more extended limb pos-
tures appears to be characteristic of larger compared to smaller ani-
mals, this trend has not been found to be consistent across all taxa,
samples have been limited, and interspecific studies may be con-
founded by phylogenetic differences among taxa (Biewener, 2015).
Ontogenetic studies can provide insight on this question because
limb postural changes associated with an increase in body size during
growth can be assessed while keeping phylogenetic influences con-
stant. Due to immature development of extensor muscles (Atzeva,
Demes, Kirkbride, Burrows, & Smith, 2007; Jouffroy & Medina, 1996),
very young animals might be expected to be characterized by more
flexed elbows and knees (Howland, Bregman, & Goldberger, 1995;
Peters, 1983; Vilensky & Gankiewicz, 1989), and only shift to using
more extended limb postures as they grow larger and achieve more
adult-like levels of muscularity (Grand, 1983). If musculature is well
developed enough to maintain extended postures, extended limb pos-
tures would be concurrently beneficial as body size increases, for the
reasons discussed above (i.e., reducing stress on limb bones, reducing
force that needs to be generated by antigravity muscles, increasing
speed, and reducing locomotor energetic costs).
A limited number of studies have tracked changes in elbow and
knee angles through ontogeny, and their results exemplify the complex-
ity of postural adjustments: forelimb posture can differ from hindlimb
posture, and fore-hind postural adjustments can differ among individu-
als (Vilensky & Gankiewicz, 1989, 1990), between males and females
(Burgess et al., 2016; Patel, Horner, Thompson, Barrett, & Henzi, 2013)
YOUNG ET AL.
3) or across species (Burgess et al., 2016; Patel et al., 2013; Young,
2009; Zeininger, Shapiro, & Raichlen, 2017). In other words, there does
not appear to be a simple, linear trajectory by which limbs start out
flexed and become more extended with age. For example, Patel et al.
(2013) found that in a cross sectional ontogenetic sample of 33 wild
baboons (Papio hamadryas ursinus) ranging in age from 12 to 108
months (body mass range 2–29.5 kg), there was postural and functional
differentiation between the fore- and hindlimbs, and between sexes;
knees became more extended as body size (age) increased (but only in
males), while elbows did not. While the flexed hindlimbs used by the
younger baboons may provide a benefit of enhanced maneuverability
(Patel et al., 2013), at larger body sizes (older individuals), postural
changes in the hindlimb were consistent with the general prediction
that larger animals use more extended joint postures to mitigate the
potential for increased stresses on the limb bones (which would be exa-
cerbated not only by increased body mass, but also by increased load
arms lengths due to rapidly growing distal hindlimb lengths). Contrary to
predictions, forelimb posture did not become more extended as age and
size increased. Rather than starting out and remaining flexed, forelimbs
started out more extended than the hindlimbs and remained consis-
tently more extended than the hindlimbs throughout ontogeny. As sug-
gested by the authors, extension of the forelimbs throughout ontogeny
would have the benefit of reducing energetic costs by increasing effec-
tive forelimb length, even at young ages (but effective limb lengths
were not reported in this study; Patel et al., 2013).
In a longitudinal ontogenetic sample of a different species of Papio
(cynocephalus) extending to much younger age ranges (2 to 9 months,
then resampled at 2–3 years; body mass range 0.774-8.9 kg) (Zeininger
et al., 2017), the elbow became slightly more extended with age, sup-
porting the general prediction of increased extension with age and body
size increase. However, unlike (male) Papio hamadryas ursinus, in which
the knee became more extended with age/size, in Papio cynocephalus,
the knee became slightly more flexed with age/size. Nevertheless, in
both species of Papio, the elbow was, at most ages, more extended than
the knee. This pattern persists in adult baboons and may be related to
the fact that hindlimbs are longer than forelimbs and more flexed hin-
dlimbs serve to equalize limb lengths (Larson et al., 2001).
In comparison to Papio hamadryas ursinus, in which forelimb exten-
sion was similar between younger and older individuals, and Papio cyn-
ocephalus, in which forelimbs were more flexed at younger ages,
ontogenetic analysis of limb posture in Saimiri boliviensis (74–302 days;
0.218–0.535 kg) unexpectedly revealed that at younger ages, squirrel
monkeys had more extended forelimbs than at older, larger ages (Young,
2009). By using extended forelimb postures, immature Saimiri were
able to shorten substrate reaction force load arms and thus mitigate
muscle force required for maintaining joint posture. This pattern, (the
opposite of the general prediction that larger animals use more
extended postures) appears to provide a behavioral compensation used
by young squirrel monkeys to circumvent ontogenetic limits on per-
formance (i.e., limited muscularity). Given the variability across species
in limb postural trends during development, future research in this area
would benefit from more detailed data addressing the ontogenetic tim-
ing of limb posture in relation to muscular development.
| 59
4.9 | Digitigrady: Insights from ontogeny
Like overall limb postures, hand and foot postures can vary across spe-
cies and throughout ontogeny. Because primates are predominantly
arboreal, most adults rely on the security of palmigrade hand postures
(full palmar surface of the hand is in contact with the substrate) com-
bined with foot postures that are either plantigrade (full plantar surface
of the foot is in contact with the substrate) or semi-plantigrade (the
heel, or heel and midfoot are elevated) (Meldrum, 1991; Schmitt & Lar-
son, 1995; Whitehead, 1993). However, like many terrestrial, cursorial
mammals, some quadrupedal primates (namely, terrestrial cercopithe-
cines) habitually or facultatively use digitigrady of the hands (in which
only the metacarpal heads and phalanges are load bearing) (Hayama,
Chatani, & Nakatsukasa, 1994; Napier & Napier, 1967; Patel, 2009;
Patel & Polk, 2010; Rollinson & Martin, 1981; Rose, 1973; Schmitt, Zei-
ninger, & Granatosky, 2016) combined with semiplantigrady of the feet
(Berillon et al., 2010; Meldrum, 1991; Schmitt & Larson, 1995). In non-
primate, cursorial mammals, digitigrady is considered to be an adapta-
tion for efficiently moving at relatively high speeds, due to its
contribution toward increasing effective limb length. Digitigrady can
also act to attenuate the effects of high substrate reaction forces asso-
ciated with faster speeds by increasing effective mechanical advantage
and reducing requisite muscle force production by limiting the joint
moments at the wrist or ankle that must be resisted by antigravity
muscles (Patel, 2009; Patel & Polk, 2010). However, manual digitigrady
in primates does not appear to be a speed-related adaptation; primates
that use manual digitigrady use it only when moving relatively slowly,
becoming more palmigrade as speed increases (Patel, 2009). Palmigrady
at higher speeds may be beneficial for distributing increased substrate
reaction forces across a broader surface area, reducing stress on the
hand (Higurashi, Goto, & Kumakura, 2017; Patel & Wunderlich, 2010).
At lower speeds, though, digitigrady in primates appears to be benefi-
cial for similar reasons to its benefits at higher speeds, serving to lower
locomotor energetic costs as long as speed is not too high (Patel, 2009,
2010; Patel, Larson, & Stern, 2012).
Due to the immaturity of the neuromuscular system early in
ontogeny, it would be reasonable to predict that the functional benefits
of digitigrady might be confined to juveniles or adults. Primate infants,
like other very young mammals, should be more likely to use palmi-
grade or plantigrade/semiplantigrade hand and foot postures which
provide stability and a broad base of support (Peters, 1983). Therefore,
one could predict that the use of digitigrade hand or foot postures
would increase as primates age, along with improvements in stability
and muscular development. If this were the case, the changes in hand
and/or foot posture through ontogeny form a natural experiment with
which to test the extent to which digitigrady contributes to increased
effective limb length (compared to contributions from extension of
other limb joints) (Patel, 2009) and to test whether or not digitigrady is
associated with increased speed.
There has been limited study of the ontogenetic development of
digitigrady among primates that use it as adults. A recent study using a
longitudinal sample of growing baboons (Papio cynocephalus) did not find
support for the prediction that the use of digitigrady would increase
60 | YOUNG
with age (Zeininger et al., 2017). Instead, while the use of palmigrady
was restricted to infants (as expected), and semiplantigrady was some-
times used at all ages, digitigrady of both the hands and feet was the
preferred posture across all ages. As in adult baboons (Patel, 2009) the
hands and feet did not become more digitigrade as velocity increased.
Extension of the elbows and knees (in combination with changes in limb
proportions during growth) contributed more strongly to increases in
effective limb length than did digitigrade postures of the hand or foot (cf.
adult Papio anubis, in which hand elevation and elbow extension both
contribute to effective limb length, but hand elevation more strongly;
Patel, 2009). Therefore, the primary functional benefit of digitigrade pos-
tures in immature baboons may be to reduce moments about the wrist
or ankle joints (Patel et al., 2012; Zeininger et al., 2017).
4.10 | Ontogeny and limb force distribution
One of the most well-known distinctive features of primate quadru-
pedalism is that—with a few exceptions (Demes et al., 1994; Schmitt,
2003a)—primates generate greater peak vertical substrate reaction
forces with their hindlimbs compared to their forelimbs, whereas the
opposite is generally true for other mammals (at least those for which
we have data) (Demes et al., 1994; Franz, Demes, & Carlson, 2005;
Hanna, Polk, & Schmitt, 2006; Kimura et al., 1979; Reynolds, 1985;
Schmitt & Hanna, 2004; Schmitt & Lemelin, 2002; Wallace & Demes,
2008). The relative reduction of vertical forces on the forelimbs is con-
sidered to have had a potentially adaptive ecological benefit for arbo-
real quadrupedal primates, freeing the forelimbs to exhibit increased
degrees of freedom and emphasizing their role in foraging and manipu-
lation over locomotor and weight support (especially on narrow flexible
substrates) (Larson, 1998). However, there is less consensus regarding
the proximate, biomechanical mechanisms by which primates achieve
hindlimb “dominance”. Three mechanisms have been proposed,
although they are not mutually exclusive (Young, 2012b). The first, the
“Center of Mass Position” model, predicts that relative magnitudes of
limb loading result from the position of the hands and feet relative to
the body’s center of mass. This model would explain the increased
forces on hindlimbs in primates as a result of the feet being closer to
the COM than the hands, regardless of whether that proximity derives
from a relatively caudally located COM or a highly protracted hindlimb,
both of which would place the feet closer to the COM than are the
hands (Gray, 1944; Raichlen et al., 2009; Rollinson & Martin, 1981).
Support for this model has come from studies of some adult primates
(e.g., Cheirogaleus medius and Pan troglodytes) (Lemelin & Schmitt,
2004; Raichlen et al., 2009), but not from others (e.g. Ateles, Cebus)
(Larson & Demes, 2011). The second mechanism is the “Active Weight
Shift” model. This model attributes increased hindlimb vertical forces to
the action of hindlimb retractor muscles acting on a protracted hind-
limb. Providing the hindlimb is stabilized, such muscle torques would
effectively “lift” the anterior trunk, resulting in an active shift of loads
from the forelimb to the hindlimb (Reynolds, 1985). Experimental stud-
ies on various primates have provided support for this model (Larson &
Demes, 2011; Larson & Stern, 2009; Reynolds, 1985). The third mecha-
nism is the “Limb Compliance” model (Schmitt, 1999; Schmitt & Hanna,
ET AL.
2004). This model predicts that primates have reduced loading on fore-
limbs relative to hindlimbs due to the more pronounced use of “compli-
ant” kinematic mechanisms (e.g., increased joint yield and support
phase duration) in the forelimb, especially on arboreal substrates, and
has also received support from experimental studies on various primate
species (Larney & Larson, 2004; Schmitt & Hanna, 2004).
Very little is known about the ontogeny of limb force distribution
among primates, despite its potential value in testing the relative impor-
tance of the three models described above. However, Young (2009,
2012b) found that in an ontogenetic sample of squirrel monkeys, limb
force distribution changed during growth, such that the monkeys transi-
tioned from being forelimb dominant to hindlimb dominant. By tracking
changes in whole body center of mass position, limb positioning, hindlimb
retractor moments at peak vertical hindlimb force, and limb compliance
(based on shoulder and hip amplitudes) during ontogeny, Young (2012b)
was able to evaluate which model (or combination of models) best
accounted for the transition in limb force distribution. He found support
for all three models, but most strongly for the COM position and Active
Weight Shift models. That is, relative increases in hindlimb vertical peak
force through ontogeny were accompanied by a caudal shift in COM
position, combined with more cranially positioned forelimbs, both of
which support the predictions of the COM model. In addition, hindlimb
retractor moments increased as the monkeys aged, along with increases
in vertical peak forces on hindlimbs relative to forelimbs, supporting the
Active Weight Shift model. Finally, forelimb compliance increased with
age, in accordance with decreases in peak vertical forces on the forelimb,
supporting the Limb Compliance model, although the trend did not reach
statistical significance, weakening support for this model. Nevertheless,
the overall results of this ontogenetic study confirm that primates may
employ more than one mechanism for limb force distribution, and sug-
gest that all three models should continue to be incorporated into adapt-
ive hypotheses about the evolution of primate quadrupedalism.
5 | CONCLUSIONS AND DIRECTIONS FOR
FUTURE RESEARCH
This analysis and review has confirmed that, as outlined and predicted
by Hurov (1991), over the last 20–30 years researchers have gained a
much greater understanding of primate locomotion by considering it
from an ontogenetic perspective. The study of primate locomotor
development has provided insights on three levels. First, it has helped
us to understand the main determinants of the timing of locomotor
independence, an important life history event. Second, it has provided
insight on locomotion from the perspective of the unique challenges
faced by infant and juvenile primates, and third, it has been effectively
used as a model system to test hypotheses regarding primate locomo-
tor functional morphology and biomechanics.
As we have illustrated, a primate’s locomotor development is inex-
tricably linked with its life history, ecology, and morphology. For exam-
ple, the timing of locomotor independence in primates is influenced by
phylogeny, adult female body mass, age at weaning, and especially rela-
tive brain size. Once primates begin locomoting independently, they
face many ecological challenges not experienced by older and larger
YOUNG ET AL.
adult group mates. Though small body size may allow juvenile primates
to engage in more acrobatic arboreal locomotion and move on smaller
substrates than adults, small body size is also a liability, due to the size-
graded nature of predation pressure. Reduced muscle mass, lack of
complete sensory-motor integration, and general musculoskeletal
immaturity also present unique ecological challenges to growing prima-
tes. Yet growing primates appear to gain some performance benefits
from allometries inherent in the morphological growth process itself—
primates, like many other mammals, exhibit negative allometric scaling
during ontogeny in muscle mechanical advantage, bone strength, and
grasping morphology of the hands and feet. Greater mechanical
advantage compensates for reduced muscular force output, greater
bone robusticity reduces fracture risk and improves safety factor,
whereas larger extremities with relatively long digits enhance grasping
span when holding onto a caregiver during transport or to an arboreal
support during independent postural or locomotor activities.
Most of the research that has used locomotor ontogeny as a
model system, or “natural experiment”, has been focused on primate
quadrupedalism, and that is what we have emphasized in our discus-
sion. However, the same approach could be used to understand form-
function links characterizing other types of primate locomotion, such as
leaping and brachiation. By tracking ontogenetic transitions in gait pat-
terns, kinematics, and kinetics, along with corresponding ontogenetic
transitions in morphology, research has demonstrated how primate
quadrupedalism is influenced by body mass distribution, whole-body
center of mass position, and limb proportions, but also by the complex
interaction of limb proportions with limb joint posture and limb excur-
sion patterns (i.e., limb placement). From this perspective we have
gained a better understanding of the key features that contribute to
primates’ long strides and low stride frequencies, use of diagonal
sequence versus lateral sequence gaits, hindlimb dominance in force
distribution, characteristic use of more extended limb postures, as well
as the (less common) use of digitigrady. These studies form a critical
foundation for assessing the selective factors that might have played
an important role in primate locomotor evolution.
Interest in primate locomotor development has grown tremendously
in the past few decades, as evidenced by the wealth of valuable contri-
butions discussed here. Given the significance of locomotor ontogeny to
our broader understanding of primate adaptation and evolution, we pre-
dict that this area of research will continue to (pardon the pun), grow
and mature. Future research would benefit from more field data on pri-
mate locomotor development and more detailed study of infant trans-
port costs across all primates. It would also be fruitful to evaluate
primate morphological growth patterns in a broad comparative context—
for example, to those of other mammals that are more terrestrially
adapted and/or more precocial. In lab-based locomotor studies, we need
more research on locomotor behaviors other than quadrupedalism (e.g.
leaping, brachiation, climbing), and for quadrupedalism, research on how
developing primates navigate non-horizontal substrates, or substrates
that vary in diameter. Future research in this area, combined with mea-
surement of the COM would prove useful in further testing the relation-
ship between body mass distribution and gait, and for sorting out the
relative influences of body size, substrate type, and age on gait
| 61
preferences and kinematics (e.g., Shapiro & Young, 2012; Shapiro et al.,
2014). We also have little to no information on the ontogeny of gait pat-
terns in strepsirrhines or hominoids, and it would be interesting to test
how differences in the ontogenetic scaling of limb proportions among
these taxa might influence gait. In addition, lab-based research would
benefit from improved data on locomotor mechanics and performance
in growing primates. We now have methodological tools available that
have greatly increased our ability to understand locomotor functional
morphology. For example, by using inverse dynamics, combined with
technologies such as X-ray Reconstruction of Moving Morphology
(XROMM: Brainerd et al., 2010) or finite element analysis, we should be
able to determine whether the magnitude of muscle forces or bone
strain differs between immature and adult primates. Using force trans-
ducers, we can also test the prediction that young primates, for their
size, can exert greater grip force compared to older animals (Young,
Chadwell, O’neill, & Patel, 2016a). It would also be interesting to test
whether due to their unique grasping needs, infant primates exhibit less
differentiation in muscle activity in digital flexors in the hands and feet
compared to adults (Patel et al., 2015). Finally, new technologies have
now greatly improved our ability to analyze locomotor kinematics in the
^t & Vereecke, 2011; Jackson, Evangelista, Ray, & Hedrick,
field (D’Aou
2016; Stevens & Carlson, 2008; Theriault et al., 2014), allowing us to
evaluate better than ever before how ontogeny, locomotor morphology,
ecology and biomechanics intersect in the context of natural habitats.
ACKNOWLE DGME NTS
We are indebted to the many individuals who have facilitated our
research on primate locomotor ontogeny at various institutions, including
the Southwest National Primate Research Center, Center for Neotropical
Primate Research and Resources, UT MD Anderson Cancer Center,
Northeast Ohio Medical University, University of Texas at Austin, and
Stony Brook University. Our ontogenetic research has been funded by
NSF (BCS-031382 and BCS-0647402 to LJS, Graduate Research Fellow-
ship to JWY) and the Leakey Foundation. Special thanks to Dave Raichlen
for his collaboration on the baboon project and discussions on the manu-
script. We also thank Trudy Turner and Chris Vinyard for encouraging us
to submit this paper for the Yearbook of Physical Anthropology, as well
as Nathan Thompson, Chris Vinyard and three anonymous reviewers for
insightful comments that improved the manuscript.
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How to cite this article: Young JW, Shapiro LJ. Developments
in development: What have we learned from primate locomotor
ontogeny?. Am J Phys Anthropol. 2018;165:37–71. https://doi.
org/10.1002/ajpa.23388