Volume 95, No.

4 THE QUARTERLY REVIEW OF BIOLOGY December 2020

BEYOND EQUILIBRIA: THE NEGLECTED ROLE

OF HISTORY IN ECOLOGY AND EVOLUTION

Hamish G. Spencer
Department of Zoology, University of Otago
Dunedin 9056 New Zealand
e-mail: hamish.spencer@otago.ac.nz

keywords
chance, chaos, constraint, construction, contingency, decider, history,
progression, modeling, template, time, turnover

abstract
Research in ecology and evolution today often emphasizes an equilibrium view of dynamical systems,
to the point where historical explanations are largely ignored. Such views are especially prominent in the
mathematical modeling of such systems where “solving” a model means finding and characterizing the
stability of its equilibria. I argue that history is far too important in biology to be discounted in this way. I
then outline a number of different “flavors” of history, by which I mean potentially overlapping ways in
which history can play a critical role in biological processes. I illustrate these flavors with examples from
the ecological and evolutionary literature, and demonstrate that adding an explicitly historical perspective
leads to a deeper understanding of the relevant biology.

Introduction Biological history, in the sense of a time-

T HE 19th-century intellectual forebears

of today’s ecologists and evolutionary
biologists were (and are) called natural histo-
rians. Nowadays, however, few professional
scientists aspire to be portrayed so: the phrase
“natural history” has an almost pejorative
tone, suggesting a level of amateurism that
is 100 years or more behind the times (see
Futuyma 1998 for an elegant refutation of
this view). Even though the word “history”
as used in “natural history” has the unusual
meaning of a systematic description, not nec-
essarily with any time component, this nega-
tive view sometimes extends to any mention
of history within biology.
dependent explanation, is surprisingly rare
science, especially in the mathematical mod-
els used in theoretical ecology and evolution.
For example, historian of science Sharon E.
Kingsland, in her illuminating analysis of the
development of ecological modeling, argued
that the mathematical ecologists of the 1960s
eschewed history because they felt it smacked
of particularities and allowed few generali-
zations (Kingsland 1985). But being able to
distill the essence of a system into principles
that apply elsewhere—generalizing—is highly
prized in science. This disparaging attitude to-
ward historical accounts remains widespread:
although we all acknowledge the importance

The Quarterly Review of Biology, December 2020, Vol. 95, No. 4

Copyright © 2020 by The University of Chicago. All rights reserved.
0033-5770/2020/9504-0002$15.00

311
312 THE QUARTERLY REVIEW OF BIOLOGY
of biological history to our favorite study sys-
tem, the inclination is often to omit it from
our models and explanations, writing it off as
contingency, unpredictable by any law. In-
stead, we focus on the equilibrial properties
of the system, or sometimes its steady state.
In this paper, I argue that history is fun-
damentally important to our understanding
of ecology and evolution, and we would do
well to look “beyond the equilibrium” when
we gauge the behavior of our study systems.
I start by showing that history has a number
of subtly different flavors, many of which
do allow generalizations and follow scientific
laws. Nevertheless, these flavors are not al-
ways distinct, and more than one can play
a part in a single biological system. In adum-
brating this taxonomy, I note that none of
this richness is apparent when we restrict our
investigations to equilibria or steady states.
Consequently, a serious consideration of the
different impacts of the history on our sys-
tem, not just describing its equilibria or steady
states, contributes to a deeper understanding.
In short, a more inclusive and yet nuanced
view of history would benefit much ecologi-
cal and evolutionary thinking.
History as Contingency
Perhaps the commonest meaning of his-
tory in a biological context has to do with
the occurrence of events conditional on a
vast array of properties of the system in ques-
tion. The dominant opinion seems to be that
what happened in the past was contingent on
so many actors and their actions that predict-
ing what happened would have been impossi-
ble. Could a mathematical model, rich with
life-history parameters and state variables,
have predicted the success of the 1860s in-
troduction to New Zealand of the yellowham-
mer (Emberiza citrinella) and the continued
rarity of its congener, the cirl bunting (E. cir-
lus), in the same places (MacLeod et al. 2005;
Pipek et al. 2015)? Maybe we can account for
this difference with the wisdom of hindsight,
but such an explanation is likely to be specific
to this particular question and will not spawn
any useful general principles. When asked to
explain the differential success of these two
Volume 95
introductions, we are reduced to a list of
particularities.
Of course, this problem with contingency
is not confined to the past: when we look at
some biological systems today, working out
where it will be tomorrow is well nigh impos-
sible. What, for example, would our model
predict if the ortolan bunting (E. hortulana)
were introduced? The outcome would de-
pend on a vast array of parameter values as
well as the current state of critical variables.
If we got some of these model features wrong,
the outcome would likely be very different;
the model cannot be usefully accurate. In-
deed, because nothing general would come
out of such a model, it seems more descrip-
tive, the very essence of “natural history.”
Yet the effect of contingency can be stud-
ied—quantified even—with mathematical
models. In optimal-foraging theory, for in-
stance, much effort has gone into under-
standing how differences in competitive
ability affect the way animals distribute them-
selves in patchy environments. A well-known
example (Parker and Sutherland 1986; Mi-
linski 1988) involves 12 fish, six of which can
obtain twice as many resources as the others,
and two feeding sites, one twice as productive
as the other. An equilibrium-centered, ahis-
torical view (Houston and McNamara 1988)
assessed the likelihood of the different ways
the fish could distribute themselves over the
two sites by calculating the number of various
combinations of good and poor competitors
that matched the total consumption at each
site to the available food. This analysis sug-
gests that the most likely distribution is for
eight fish, four good and four poor competi-
tors, to be at the better site and the remaining
two of each competitive class to be at the
poorer site (see Figure 1). If, however, the
fish arrive in a random order and make indi-
vidual decisions about which site offers the
better reward, it is more likely that the better
site will have just seven fish in all, five good
competitors and two poor ones (Spencer
et al. 1995). The distinction is crucial because
the distribution of the number of fish under-
matches that of the resources (Figure 1), a
finding common but often unnoticed in ex-
periments (Kennedy and Gray 1993). Thus,
not only do the ahistorical and historical
December 2020 ROLE OF HISTORY IN ECOLOGY AND EVOLUTION 313

Figure 1. The Likelihood of the Different Outcomes of the Distribution of Fish in a Patchy Environment
The large fish consume twice as many resources as the small ones; the habitat on the left has twice as many
resources as that on the right. The resources on each side match the consumption on each side in all four sce-
narios shown. The Ideal Free Distribution (IFD) describes the situation when there are twice as many fish on the
left as on the right; undermatching occurs when there are fewer fish at the richer site than expected under the
IFD, overmatching when there are more. An ahistorical approach to estimating the likelihood of the different
distributions looks at the fraction of possible combinations of large and small fish in each scenario. This calcu-
lation implies the IFD-matching solution is by far the most likely, because it affords more possible combinations.
If, instead, we assemble the system over time, introducing individual fish randomly and allowing them to choose
the richer resource contingent on the fish already there, the undermatching 7:5 ratio is the most likely. See
Spencer et al. (1995) for details. See the online edition for a color version of this figure.

approaches give different answers to the ways
in which the fish will likely be distributed, but
the latter, by incorporating contingency and
chance, explains a counterintuitive empirical
observation.
A second illustration is given by the vexed
issue of the relative contributions of major
genes versus many polygenes of small effect
to a population’s response to natural selec-
tion. Building on the previous theoretical
work of Lande (1983), Gomulkiewicz et al.
(2010) modeled a population possessing both
sorts of genetic variation that invades a harsh
new environment. In a particularly interest-
ing example, they assumed (as is often the
case) that the originally uncommon major
allele had significant negative pleiotropic ef-
fects in addition to its positive consequences
in the new environment. At equilibrium, they
found that major allele was extinct; the re-
sponse was all down to polygenes. Neverthe-
less, the initial response of the population
was due mostly to increases in the frequency
of the major allele, which was later driven to
extinction by its pleiotropic effects, as the poly-
genic response slowly facilitated adaptation.
Critically, a population lacking such major-
gene variation was at risk of extinction upon
entering this harsh environment, since its
initial polygenic response would likely be in-
adequate. In summary, successful polygenic
adaptation can be contingent on transient
major-gene variation.
History as Chance
An even less well-behaved version of his-
tory as contingency adds stochasticity to the
equation. Anything contingent on random
events becomes impossible rather than merely
difficult to predict. Genetic drift, for instance,
ensures that isolated populations of the same
314 THE QUARTERLY REVIEW OF BIOLOGY
species will become genetically differentiated
even in identical environments. If and when
the environment does change, any conse-
quent natural selection will have in these pop-
ulations different material on which to work.
It is important to distinguish between his-
tory as contingency and history as chance.
Biological modelers often subsume complex
aspects of contingency into random elements,
glossing over the exact reasons—or perhaps
ignorant of them—for small deviations from
the predicted outcome. Countless papers con-
tain an equation with a final term “+ ε” where
ε is normally distributed with mean zero and
some small variance. Tellingly, this addition is
invariably known as the “error” and is placed
at the very end of the line, almost as an after-
thought. Nevertheless, contingency, being
deterministic, is conceptually different from
random chance.
Admittedly, discriminating contingency
from chance is not always straightforward.
The competitive-fish example above might
seem like chance, because in the historical
models the fish are introduced into the sys-
tem in a random order. But any two simula-
tions of the model in which the fish arrive
Figure 2. Chaotic Behavior in a Deterministic System
The iterations over time for Equation (1) with a = 3:8 and x0 = 0:5. Note that there is no discernible period to
the iterations.
Volume 95
in the same order will give the same result.
The choice made by the model fish is com-
pletely deterministic, contingent only on which
fish are already at each site.
History as Chaos
Even deterministic systems can behave
quite unexpectedly, a property mathemati-
cians call chaos (Li and Yorke 1975). Cru-
cially, chaotic systems need not be at all
complicated: the recursion equation
xt+1 = ax t ð1 − xt Þ (1)
is chaotic if a = 3:8, for example (May 1975;
see Figure 2). Note that Equation (1) is one
version of the well-known logistic difference
equation for population growth. (Perhaps
the more usual formation of this equation
is Nt+1 = Nt ð1 + r ð1 − Nt =K ÞÞ. Equation (1)
can be recovered, however, by defining xt =
r =ð1 + r ÞðNt =K Þ and a = 1 + r .)
In the defining feature of chaotic systems,
the state variable of the system (the value of
xn+1 in our equation) does not approach an
equilibrium. Instead, the values either cycle
among a certain number of values (this
December 2020 ROLE OF HISTORY IN ECOLOGY AND EVOLUTION
number being the “period” of the cycle, and
any number is possible) or, far more likely,
iterate around completely different values
(effectively a cycle of infinite period). This be-
havior is not unpredictable (since the equa-
tion can tell us exactly what value we will get
next if we know exactly where we are now),
but it is close. This predictability is important,
because it has allowed the development of
analytical tools that enable short-term pre-
diction (e.g., Sugihara and May 1990). Finally,
chaotic systems are not merely mathemati-
cal esoterica: for example, measles epidem-
ics exhibit chaotic dynamics (Sugihara and
May 1990).
History as Capriciousness
Part of the reason for ignoring ecological
and evolutionary history may be the sense that
it is too fickle for proper scientific study. Pop-
ulation geneticist Richard Lewontin (1966)
was one of the first to demonstrate the con-
sequences of history that did not involve
chance or chaos in his computer simulation
of temporally varying viability selection at a
single locus. Exactly the same selection pres-
sures presented in a different order caused
utterly different allele-frequency dynamics.
Worse, this deterministic system behaved more
unexpectedly than a truly stochastic one be-
cause it did not even follow the usual statistical
rules, such as the “Law of Large Numbers.”
This law states that as our sample size increases,
our knowledge of the system also increases.
As a concrete example, for most statistical dis-
tributions, the means of larger samples are
closer to the true mean of the distribution.
Lewontin termed this behavior “capricious.”
The failure to behave in a statistically reliable
way—“things do not average out”—is what
distinguishes capriciousness from chance
and contingency.
History as Approach
The apparent lack of generality engen-
dered by these versions of history led mathe-
matical ecologists to develop the ahistorical
outlook that prevails today, not only in ecol-
ogy, but also in population genetics. Kingsland
(1985) noted that this view emphasizes the
315
equilibrial behavior of its systems, the proper-
ties of the fixed points of the model equations,
possible locations of the system when history
is finished. Such a perspective is particularly
amenable to mathematical techniques (and,
indeed, for that reason was inherent in much
early mathematical biology), but it can close
our eyes to some of the ways we can improve
our understanding of biology.
To give a nonecological example, in ex-
plaining why deleterious mutations (such as
that leading to Tay-Sachs disease) are ever
found in natural populations, almost all text-
books (e.g., Nielsen and Slatkin 2013) quote
the formula for the so-called “mutation-se-
lection balance”pfrequency
ffiffiffiffiffiffiffi
of a deleterious
recessive allele, m=s (in which m is the mu-
tation rate from the wild-type allele to the
mutant and s is the selection coefficient
against the homozygous recessive). Yet al-
most never do these same textbooks note
that the rate of approach to this equilibrium
value is painfully slow (and so the observed
frequency in any real population may not
be an equilibrium and parameter estimates
derived from this frequency, assuming it is,
may be inaccurate). This tardiness should
not be confused with the additional effect
of genetic drift, which, in finite populations,
produces small random changes in the fre-
quency of the mutation. In small populations,
especially, drift lowers the mean frequency
(Wright 1937), and so the deterministic equi-
librium value given by the standard formula
may never be attained, nor will this value be
the average over time.
So not only is history completely over-
looked by our textbooks but, perhaps more
importantly, the likelihood that the system is
not at equilibrium yet (and so the mutation
is significantly rarer or commoner than pre-
dicted) is ignored. Indeed, the way the mod-
els are usually presented never even raises
in our minds the possibility of history: “solv-
ing” the model means finding the equilibria
(and possibly characterizing these points as
unstable, locally or globally stable).
Ironically, all is not lost—we can include
history, say, “history as the approach toward
an equilibrium”—even if we insist on a math-
ematical treatment. The speed at which a pop-
ulation progresses toward the equilibrium
316 THE QUARTERLY REVIEW OF BIOLOGY
allele frequency is easily calculated (by con-
sidering the difference between the leading
eigenvalue and unity). Nevertheless, this ver-
sion of history is rather weak: we are simply
waiting for the end of history, when the equi-
librium is reached.
History as Constraint
The way in which history can act as a con-
straint on evolution and ecology is similar to
its contingent role. They differ in that con-
tingency (at least as I have used it here) is
about the consequences of the actors who
happen to be present in the current system,
whereas constraint is about what has already
taken place to build the system. By seriously
considering the constraining nature of his-
torical events (rather than dismissing them
as ungeneralizable), we can often gain con-
siderable insight.
Consider, as an example, the reduction in
genome size of a number of eubacteria living
in specialized environments, such as the cy-
toplasm of various invertebrate species. Buch-
nera in aphids and Wolbachia in a wide variety
of arthropods come to mind (Correa and
Ballard 2016; Gil and Latorre 2019). These
organisms have evolved from ancestors with
much larger genomes and we can learn much
about essential gene function by seeing which
parts of the genome have been eliminated in
the course of their evolution (Wernegreen
2017).
The simplest approach to this question was
naively ahistorical: we could elucidate which
genes are indispensable by compiling a list
of those that are present in all such eubac-
teria. Very quickly, however, this catalog of
critical genes became far too small, approxi-
mately 80 (Koonin 2000). Clearly, different
lineages have taken different paths toward
a minimal genome, often satisfying the same
functional requirement with nonhomologous
genes. History really matters here: which
genes are eliminated is constrained by what
has already gone (Moran 2002). Indeed, two
flavors of history are acting in concert in this
example. Because the genetic machinery en-
abling different aspects of metabolic func-
tion can be shared among different long-term
endosymbionts (and sometimes the host it-
Volume 95
self ), genomic reduction may also be con-
tingent on which other endosymbionts are
present within the host (Douglas 2016).
History as Construction
Focusing on the process of how biological
systems evolve or are constructed over time in-
volves a realization that the equilibrial prop-
erties are an incomplete—and sometimes
misleading—summary of the way the system
behaves. This change of viewpoint can be crit-
ical in answering some of the more enduring
questions in both ecology and evolutionary
biology that have to do with the persistence
of variation: Why do we see so many species
in natural ecosystems (May 1973)? Why do
we see so many alleles in natural populations
(Lewontin 1974)?
The ahistorical approach to these questions
led to a conundrum: the parts of mathemati-
cal parameter space affording multispecies
communities (May 1973) or selectively main-
tained multiallele polymorphisms (Lewontin
et al. 1978; see Figure 3a) are miniscule. In
the latter case, these results were (and are)
widely held to mean that natural selection
could not maintain large numbers of alleles
(e.g., Kimura 1983; Charlesworth 2006; Glo-
ria-Soria et al. 2012; Ejsmond et al. 2014;
Radwan et al. 2020). But this inference is a
logical fallacy. Quite generally, the magni-
tude of some fraction of parameter space tells
us almost nothing about the likelihood that
real parameters actually occur there (Spen-
cer and Chiew 2015).
Incorporating history into these models,
by letting new species invade a community
(Taylor 1988) or novel mutations arise in a
population (Spencer and Marks 1988; Marks
and Spencer 1991; see Figure 3b) one at a
time, resolved the paradox (and revealed the
logical error). These “constructionist” models
(Taylor 2005) showed that the tiny variation-
preserving parts of parameter space were com-
monly reachable via a natural process (species
invasion and population dynamics, and mu-
tation with selection, respectively). In other
words, stable multispecies communities and
selectively maintained multiallele polymor-
phisms are easily constructed over time. I has-
ten to point out that there are other legitimate
December 2020 ROLE OF HISTORY IN ECOLOGY AND EVOLUTION 317

Figure 3. Ahistorical and Historical Models of the Likelihood of Single-Locus Polymorphisms

a. The proportion of random sets of constant viabilities that afford full polymorphism for different numbers
of alleles (after Lewontin et al. 1978). b. The distribution of the number of alleles after 10,000 generations of
a constructionist simulation of the single-locus constant-viability model of selection (after Marks and Spencer
1991). See the online edition for a color version of this figure.

reasons why selection may not actively main-
tain genetic polymorphisms, but the small size
of the relevant parts of parameter space is not
one of them.
But perhaps the most important conse-
quence of including historical construction
into the mathematical modeling has been
the ongoing fruitful areas of investigation that
would never have been possible without such
a perspective. For instance, Maynard et al.
(2018) have shown that a number of patterns
observed in ecological networks are not se-
lected directly. Rather they are the incidental
consequences of the process of community as-
sembly, so called “spandrels” sensu Gould and
Lewontin (1979). In an example from popu-
lation-genetic theory, Trotter and Spencer
(2008) showed that sufficiently fit mutant
alleles could always invade a population gov-
erned by a very general model of frequency-
dependent selection. In a sense, then, such
populations never reach equilibrium; histor-
ical construction is never-ending.
History as Turnover
In spite of the exclusively equilibrial view of
many mathematical models in biology, some
biological theories have always contained
some explicit history. The highly mathemat-
ical neutral theory of molecular evolution,
for instance, is overtly nonequilibrial, por-
traying genetic variation as being in everlast-
ing flux, new variation arising continually via
mutation and all alleles heading for eventual
extinction via genetic drift (Kimura 1983).
Nevertheless, even this theory emphasizes a
steady state, at which the level of genetic varia-
tion (measured, for example, by heterozygos-
ity) reaches an equilibrium value. In ecology,
the theory of island biogeography (Mac-
Arthur and Wilson 1967) takes a similar view:
an island’s fauna is turning over in perpetuum,
but local extinctions are matched by restock-
ing with immigrants to give an equilibrium
level of species diversity. Hence, it could be ar-
gued that neither of these emphases is truly
historical because the emphasis remains equi-
librial. Nevertheless, both of these theories do
allow a genuine historical perspective. For ex-
ample, once a steady state has been reached,
we can calculate the expected distribution of
heterozygosity under neutrality instead of just
the mean of the distribution. Even the steady-
state requirement can be relaxed: we can also
examine the path heterozygosity takes on its
way to the steady state (Nei et al. 1975). Both
of these theories have the virtue of causing us
to ask whether our biological system is (or can
ever be) at equilibrium, a question that can
easily be overlooked.
History as Template
Even the uniqueness of a single historical
contingency does not preclude its scientific
318 THE QUARTERLY REVIEW OF BIOLOGY
analysis or modeling. Such events can be in-
vestigated using phylogenetic methods, for
example, allowing us to view them as provid-
ing evolution with a template on which to
work. An increasingly common approach in-
volves deriving, from a set of, say, molecular
data, a confident estimate of the phyloge-
netic history of the group of interest and then
mapping a second data set, say, of morphol-
ogy or behavior, onto this tree. Instead of dis-
missing the origin of a particular feature as
irreducibly contingent (or worse, telling an
ad hoc just-so story about it), we can see from
what it was derived and into what it later
evolved. For instance, hypotheses concerning
the evolution of social displays involved in
courtship of the cormorants and their rela-
tives were able to be tested by mapping these
behaviors onto phylogenetic trees based on
morphological and genetic data (Kennedy
et al. 1996). In turn, this mapping anticipated
that the pied cormorant (Phalacrocorax va-
rius) stretched its neck upward during the
gape display, a prediction that was subse-
quently verified. A similar use of phylogenies
to illuminate unique historical events such as
host shifts in parasites involves comparing
the evolutionary trees of hosts and their para-
sites. For example, Johnson and Clayton (2003)
showed that the wing lice that parasitize pi-
geons and doves have done so for a much
longer time than these birds’ body lice. By
necessity, explanations of unique historical
events are particular to a single biological sys-
tem (cormorant behaviors; lice and pigeon
coevolution); what is general is, of course,
the method.
Why Does All of This Matter?
Most fundamentally, a proper consider-
ation of the different flavors of history leads
to a deeper understanding of that history.
To give a concrete example, three of these
flavors—contingency, chance, and chaos—
have been emphasized (and, I believe, con-
flated) by the late Stephen Jay Gould with
his metaphor of the “tape of life” (Gould
1989). If this tape were replayed, Gould
argued, evolution would have followed an
entirely different course. The reason why evo-
lutionary history would be different would al-
Volume 95
most certainly be due to contingency, chance,
and chaos. But I think it important to distin-
guish between these reasons because they im-
ply fundamentally different causes amenable
to different lines of investigation. Contingent
events need not be chaotic, nor are chaotic
processes governed by chance. In the case of
the tape of life, was the course of evolution
dependent on, for example, the interactions
of particular species that may or may not have
been present in the biota of certain regions
(contingency), the particular mutations that
occurred in the genomes of ancestral taxa
(chance), or the particular values of spe-
cies’ population sizes (potentially chaotic).
Of course, almost certainly, all three of these
flavors of history were involved.
Sorting out which flavors were critical at
particular times, while scientifically challeng-
ing, vastly improves our explanations, not only
of what happened, but also of what did not
happen. A good example is given by Raup
and Gould (1974), who showed that what
appear to be selectively driven directional
evolutionary changes that built on contingent
events may instead be the consequences of
chance. This paper was, in fact, an explicit at-
tempt to move that most historical and partic-
ularist of evolutionary sciences, paleontology,
toward explanations that were statistically ro-
bust and generalizable.
Furthermore, de-emphasizing the equi-
librium-focused approach to modeling can
open our eyes to aspects of the problem that
we may otherwise have never considered. For
example, the constructionist evolutionary sim-
ulations discussed above raised the previously
unforeseen question of why any loci should
be monomorphic, given how easily polymor-
phisms arose (Spencer and Marks 1988). In
the case of the loss of genes in the insect en-
dosymbionts, having a historical view raises
questions about whether losses might have
occurred in different orders and which genes
might be lost in the future (Wernegreen 2017).
The application of phylogenetic methods to
the study of hosts and their parasites rejuve-
nated the field of coevolution, so that now
we ask new questions about, for instance, the
rates at which parasites “miss the boat” during
range-expanding colonization events (e.g.,
MacLeod et al. 2010) or which host tree
December 2020 ROLE OF HISTORY IN ECOLOGY AND EVOLUTION
topologies have more infected species (e.g.,
Engelstädter and Fortuna 2019).
Thinking “beyond the equilibrium” also
gives us a much more informed perspective.
Indeed, population biologists have known for
almost 100 years that the rate of approach to
equilibrium is actually more important than
the point itself (Fisher 1924). Yet our over-
whelming concern with equilibria (and,
undoubtedly, the relative ease with which
equilibrium value(s) can be calculated) easily
beguiles us. Consider, for instance, the pop-
ulation genetics of rare deleterious alleles
that are fully recessive. A breeding strategy
in which carriers of these alleles mated only
with homozygotes for the dominant wild-
type allele would initially lead to a great re-
duction, if not the complete elimination, of
the disadvantageous genotype, since all of the
deleterious alleles would thence be “masked”
in the heterozygous state. Such a scheme
has been practiced to reduce the incidence
of Tay-Sachs disease in ultra-Orthodox Jews
in New York City (Merz 1987). Campbell
(1987) was worried, however, that masking
would eventually lead to disastrous public-
health consequences. He pointed out that
the recessive alleles would increase in fre-
quency, reaching an equilibrium at which
masking was no longer possible and many
people would die. But Campbell’s concern
ignores the issue of how long this eventual-
ity would take. The increase is glacially slow,
driven by mutation. Paul and Spencer (1988)
estimated that the time involved was approxi-
mately one million years (more than 40,000
generations at 25 years per generation), by
which time any public-health imperatives would
likely be unrecognizable.
Going “beyond the equilibrium” really
matters from an empirical viewpoint as well.
There is an increasing recognition that many
features of numerous natural populations are
not at equilibrium, and we must incorporate
this aspect into our thinking. For example,
populations that pass through a bottleneck
lose much of their variation relatively quickly,
but it can take a very long time before the lev-
els of selectively neutral diversity build up
again to the predicted equilibrium of the
neutral theory (Nei et al. 1975; Charlesworth
2009). The effects of the bottleneck that oc-
319
curred as the ancestors of modern European
and Asian humans moved out of Africa, for
instance, remain in those populations today
(Auton et al. 2015). Torres et al. (2020) have
shown that the effects of purifying selection
in nonequilibrium populations (such as those
recovering from a bottleneck) cannot be accu-
rately modeled using classical equilibrium ap-
proaches. These nonequilibrium populations
can exhibit surprising dynamics, especially in
the short term.
In closing, I want to be clear that I am not
saying that searching for biological equilib-
ria is not worthwhile. Clearly, knowing some-
thing about the stability or otherwise of a
dynamical system is of fundamental impor-
tance. But I think we can do so much more:
it is crucial that ecologists and evolutionary
biologists incorporate a more historical per-
spective into their thinking. Such a change
is essential when a substantial number of
biological systems are not at equilibrium
(as island biogeography and neutral evolu-
tion imply); history as turnover may be all-
important. Moreover, as the competing fish
example reveals, this change would benefit
our explanations and understanding of the
natural world even if an equilibrium world-
view were correct. We may be at an equi-
librium, but how we got there determined
which one of several possibilities was real-
ized. Thinking more seriously about history
naturally entails working out what roles it
plays in our study system. My list of historical
flavors is not meant to be exhaustive; rather
it should be seen a stimulus for further inves-
tigations. And there may well be differences
between theoretical studies and empirical re-
search, or between scientific investigations in
evolution and those in ecology, in the degree
of emphasis placed on equilibria. Whatever
the case, teasing out the many roles various
different flavors of history play in nature is
much better than rolling them all into one
and dismissing it as we do “natural history.”
acknowledgments
I would like to thank Sam Elworthy, Adrian Paterson,
Sonia Sultan, and Marlene Zuk for helpful discussions
and comments. Doug Futuyma and an anonymous re-
viewer also made useful suggestions for improvements
on the paper, for which I am most grateful.
320 THE QUARTERLY REVIEW OF BIOLOGY
REFERENCES
Auton A., Abecasis G., Altshuler D., et al., 1000 Ge-
nomes Project Consortium. 2015. A global refer-
ence for human genetic variation. Nature 526:68–74.
Campbell R. B. 1987. The effects of genetic screening
and assortative mating on lethal recessive-allele fre-
quencies and homozygote incidence. American Jour-
nal of Human Genetics 41:671–677.
Charlesworth B. 2009. Effective population size and
patterns of molecular evolution and variation. Na-
ture Reviews Genetics 10:195–205.
Charlesworth D. 2006. Balancing selection and its
effects on sequences in nearby genome regions.
PLOS Genetics 2:e64.
Correa C. C., Ballard J. W. O. 2016. Wolbachia associ-
ations with insects: winning or losing against a mas-
ter manipulator. Frontiers in Ecology and Evolution
3:153.
Douglas A. E. 2016. How multi-partner endosymbioses
function. Nature Reviews Microbiology 14:731–743.
Ejsmond M. J., Radwan J., Wilson A. B. 2014. Sexual se-
lection and the evolutionary dynamics of the major
histocompatibility complex. Proceedings of the Royal
Society B: Biological Sciences 281:20141662.
Engelstädter J., Fortuna N. Z. 2019. The dynamics of
preferential host switching: host phylogeny as a key
predictor of parasite distribution. Evolution 73:1330–
1340.
Fisher R. A. 1924. The elimination of mental defect.
Eugenics Review 16:114–116.
Futuyma D. J. 1998. Wherefore and whither the natu-
ralist? American Naturalist 151:1–6.
Gil R., Latorre A. 2019. Unity makes strength: a review
on mutualistic symbiosis in representative insect
clades. Life 9:21.
Gloria-Soria A., Moreno M. A., Yund P. O., Lakkis
F. G., Dellaporta S. L., Buss L. W. 2012. Evolution-
ary genetics of the hydroid allodeterminant alr2.
Molecular Biology and Evolution 29:3921–3932.
Gomulkiewicz R., Holt R. D., Barfield M., Nuismer S. L.
2010. Genetics, adaptation, and invasion in harsh
environments. Evolutionary Applications 3:97–108.
Gould S. J. 1989. Wonderful Life: The Burgess Shale and
the Nature of History. New York: W. W. Norton.
Gould S. J., Lewontin R. C. 1979. The spandrels of
San Marco and the Panglossian paradigm: a cri-
tique of the adaptationist programme. Proceedings
of the Royal Society B: Biological Sciences 205:581–598.
Houston A. I., McNamara J. M. 1988. The ideal free
distribution when competitive abilities differ: an ap-
proach based on statistical mechanics. Animal Be-
haviour 36:166–174.
Johnson K. P., Clayton D. H. 2003. Coevolutionary his-
tory of ecological replicates: comparing phyloge-
nies of wing and body lice to columbiform hosts.
Pages 262–286 in Tangled Trees: Phylogeny, Cospecia-
Volume 95
tion, and Coevolution, edited by R. D. M. Page. Chi-
cago (Illinois): University of Chicago Press.
Kennedy M., Gray R. D. 1993. Can ecological theory
predict the distribution of foraging animals? A crit-
ical analysis of experiments on the ideal free distri-
bution. Oikos 68:158–166.
Kennedy M., Spencer H. G., Gray R. D. 1996. Hop,
step and gape: do social displays of the Pelecani-
formes reflect phylogeny? Animal Behaviour 51:273–
291, 1197 (erratum).
Kimura M. 1983. The Neutral Theory of Molecular Evolu-
tion. Cambridge (United Kingdom): Cambridge Uni-
versity Press.
Kingsland S. E. 1985. Modeling Nature: Episodes in the
History of Population Ecology. Chicago (Illinois): Uni-
versity of Chicago Press.
Koonin E. V. 2000. How many genes can make a cell:
the minimal-gene-set concept. Annual Review of Ge-
nomics and Human Genetics 1:99–116.
Lande R. 1983. The response to selection on major
and minor mutations affecting a metrical trait. He-
redity 50:47–65.
Lewontin R. C. 1966. Is nature probable or capricious?
BioScience 16:25–27.
Lewontin R. C. 1974. The Genetic Basis of Evolutionary
Change. New York: Columbia University Press.
Lewontin R. C., Ginzburg L. R., Tuljapurkur S. D. 1978.
Heterosis as an explanation for large amounts of
polymorphism. Genetics 88:149–170.
Li T.-Y., Yorke J. A. 1975. Period three implies chaos.
American Mathematical Monthly 82:985–992.
MacArthur R. H., Wilson E. O. 1967. The Theory of Is-
land Biogeography. Princeton (New Jersey): Prince-
ton University Press.
MacLeod C. J., Duncan R. P., Parish D. M. B., Wratten
S. D., Hubbard S. F. 2005. Can increased niche op-
portunities and release from enemies explain the
success of introduced yellowhammer populations
in New Zealand? Ibis 147:598–607.
MacLeod C. J., Paterson A. M., Tompkins D. M., Dun-
can R. P. 2010. Parasites lost—do invaders miss the
boat or drown on arrival? Ecology Letters 13:516–527.
Marks R. W., Spencer H. G. 1991. The maintenance of
single-locus polymorphism. II. The evolution of fit-
nesses and allele frequencies. American Naturalist
138:1354–1371.
May R. M. 1973. Complexity and Stability in Model Ecosys-
tems. Princeton (New Jersey): Princeton University
Press.
May R. M. 1975. Biological populations obeying differ-
ence equations: stable points, stable cycles, and
chaos. Journal of Theoretical Biology 51:511–524.
Maynard D. S., Serván C. A., Allesina S. 2018. Network
spandrels reflect ecological assembly. Ecology Letters
21:324–334.
December 2020 ROLE OF HISTORY IN ECOLOGY AND EVOLUTION
Merz B. 1987. Matchmaking scheme solves Tay-Sachs
problem. Journal of the American Medical Association
258:2636, 2639.
Milinski M. 1988. Games fish play: making decisions
as a social forager. Trends in Ecology and Evolution
3:325–330.
Moran N. A. 2002. Microbial minimalism: genome re-
duction in bacterial pathogens. Cell 108:583–586.
Nei M., Maruyama T., Chakraborty R. 1975. The bot-
tleneck effect and genetic variability in popula-
tions. Evolution 29:1–10.
Nielsen R., Slatkin M. 2013. An Introduction to Popula-
tion Genetics: Theory and Applications. Sunderland (Mas-
sachusetts): Sinauer Associates.
Parker G. A., Sutherland W. J. 1986. Ideal free distribu-
tions when individuals differ in competitive ability:
phenotype-limited ideal free models. Animal Behav-
iour 34:1222–1242.
Paul D. B., Spencer H. G. 1988. Genetic screening and
public health. American Journal of Human Genetics
43:344–346.
Pipek P., Pyšek P., Blackburn T. M. 2015. How the yel-
lowhammer became a Kiwi: the history of an alien
bird invasion revealed. NeoBiota 24:1–31.
Radwan J., Babik W., Kaufman J., Lenz T. L., Winter-
nitz J. 2020. Advances in the evolutionary under-
standing of MHC polymorphism. Trends in Genetics
36:298–311.
Raup D. M., Gould S. J. 1974. Stochastic simulation
and evolution of morphology—towards a nomo-
thetic paleontology. Systematic Zoology 23:305–322.
Spencer H. G., Chiew K. X. 2015. The maintenance of
single-locus polymorphism by maternal selection.
G3: Genes, Genomes, Genetics 5:963–969.
321
Spencer H. G., Marks R. W. 1988. The maintenance of
single-locus polymorphism. I. Numerical studies of
a viability selection model. Genetics 120:605–613.
Spencer H. G., Kennedy M., Gray R. D. 1995. Patch
choice with competitive asymmetries and percep-
tual limits: the importance of history. Animal Be-
haviour 50:497–508.
Sugihara G., May R. M. 1990. Nonlinear forecasting as
a way of distinguishing chaos from measurement
error in time series. Nature 344:734–741.
Taylor P. J. 1988. The construction and turnover of
complex community models having generalized
Lotka-Volterra dynamics. Journal of Theoretical Biol-
ogy 135:569–588.
Taylor P. J. 2005. Unruly Complexity: Ecology, Interpretation,
Engagement. Chicago (Illinois): University of Chi-
cago Press.
Torres R., Stetter M. G., Hernandez R. D., Ross-Ibarra J.
2020. The temporal dynamics of background
selection in nonequilibrium populations. Genetics
214:1019–1030.
Trotter M. V., Spencer H. G. 2008. The generation
and maintenance of genetic variation by frequency-
dependent selection: constructing polymorphisms
under the pairwise interaction model. Genetics 180:
1547–1557.
Wernegreen J. J. 2017. In it for the long haul: evolu-
tionary consequences of persistent endosymbiosis.
Current Opinion in Genetics & Development 47:83–90.
Wright S. 1937. The distribution of gene frequencies
in populations. Proceedings of the National Academy
of Sciences of the United States of America 23:307–320.
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