Gene-culture coevolution in the age of genomics

Peter J. Richerson
a,1
, Robert Boyd
b
, and Joseph Henrich
c
a
Department of Environmental Science and Policy, University of California, Davis, CA 95616;
b
Department of Anthropology, University of California, Los
Angeles, CA 90095; and
c
Departments of Psychology and Economics, University of British Columbia, Vancouver, BC V6T 1Z4, Canada
The use of socially learned information (culture) is central to human
adaptations. We investigate the hypothesis that the process of
cultural evolution has played an active, leading role in the evolution
of genes. Culture normally evolves more rapidly than genes,
creating novel environments that expose genes to new selective
pressures. Many human genes that have been shown to be under
recent or current selection are changing as a result of new environ-
ments created by cultural innovations. Some changed in response to
the development of agricultural subsistence systems in the Early and
Middle Holocene. Alleles coding for adaptations to diets rich in plant
starch(e.g., amylase copy number) and toepidemic diseases evolved
as human populations expanded (e.g., sickle cell and G6PD de-
ciency alleles that provide protection against malaria). Large-scale
scans using patterns of linkage disequilibriumto detect recent selec-
tion suggest that many more genes evolved in response to agricul-
ture. Genetic change in response to the novel social environment of
contemporary modern societies is also likely to be occurring. The
functional effects of most of the alleles under selection during the
last 10,000 years are currently unknown. Alsounknown is the role of
paleoenvironmental change in regulating the tempo of hominin
evolution. Although the full extent of culture-driven gene-culture
coevolutionis thus far unknownfor the deeper history of the human
lineage, theory and some evidence suggest that such effects were
profound. Genomic methods promise to have a major impact on our
understanding of gene-culture coevolution over the span of homi-
nin evolutionary history.
cultural evolution
|
human evolution
|
Pleistocene
|
recent selection
T
he human cultural system supports the cumulative evolution
of complex adaptations to local, often ephemeral environ-
ments. Using elaborate technology and depending on large
bodies of cultural knowledge about plants and animals, stone-age
foragers spread to a much wider range of habitats than any other
mammal, from the frigid tundra in the Arctic to the arid deserts
of Australia. The Polynesian outrigger canoe and the Arctic
kayak are examples of the astoundingly sophisticated cultural
adaptations that people have used to occupy distant corners of
the globe. The forms of social organizations observed in humans
are more diverse than the rest of the primate order combined.
Humans constitute one of the worlds most impressive adaptive
radiations. We have occupied virtually every habitat on earth by
using technology and social organization to generate thousands
of socioeconomic systems (1, 2).
Cultural Evolution and Gene-Culture Coevolution
Culture has many denitions, but for our purposes a useful one is
all of the information that individuals acquire from others by
a variety of social learning processes including teaching and
imitation (3). Transmission delity is often sufciently high for
culture to act as an inheritance system (4). We commonly ob-
serve that the ideas, practices, skills, attitudes, norms, art styles,
technology, ways of speaking, and other elements of culture
change through time, but we also see that persistent traditions
exist. The English of Shakespeare is plainly a recent ancestor of
the language spoken in England today, but modern English
speakers cannot fully appreciate his plays without some knowl-
edge of the differences between Elizabethan and modern En-
glish. Culture is thus a system of descent with modication. The
idea that culture is fundamentally a kind of inheritance system
that can be investigated using population thinking has been
very productive. It led evolutionary theorists to model cultural
evolutionary process by drawing tools and inspiration from elds
as diverse as population genetics, epidemiology, ecology, game
theory, and stochastic processes (3, 5).
Those familiar with genetic evolution may be aided by consid-
ering some of the similarities and differences between genetic and
cultural evolution. Key differences include the nature of forces that
act on cultural transmission, the observed patterns of transmission,
and the relative rates of adaptation. Several of the forces that act
on cultural variation to cause cultural evolutionary change include
ones familiar to evolutionary biologists, such as random errors in
teaching or acquiring items of culture (mutation), statistical effects
in small populations (drift), and the effects on an individuals life
chances as a consequence of using different cultural variants
(natural selection). Other forces on cultural evolution are dis-
tinctive and derive from the fact that the acquirers of culture, even
infants, are choice-making agents. People can to some extent pick
and choose from among the different cultural variants they ob-
serve. Assuming their choices are not random, this creates a variety
of bias forces that can be dened by how the choices are made (6).
Humans also selectively transmit variants that they have learned to
their offspring and to others. We call such psychological processes
decision-making forces. Parentoffspring transmission domi-
nates much (although not all) genetic transmission. In contrast,
evidence on transmission patterns from a variety of sources indi-
cates that individuals, including both children and adults, learn
from a large, dynamic social network including parents, siblings,
peers, and a wide range of others. The social learner uses biases
that focus attention on those who tend to be same-sex, same-
ethnicity, older, successful, prestigious, and available in order to
accumulate a cultural repertoire from their social networks (79).
Humans also generate new variants by nonrandom processes such
as individual learning and creative thinking.
Field evidence on adaptive rates shows that they can be much
faster for cultural evolution compared with genetic evolution (1,
10). For example, when American sweet potatoes tolerant of cool
weather became available to the peoples of Highland New
Guinea, the new crop set off a population explosion and a spurt of
parallel social and economic innovations in a number of Highland
societies (11). Attractive gadgets, such as mobile phones, have
been taken up avidly around the contemporary world, and many
of them lead to important knock-on cultural changes. The upshot
of the differences between cultural and genetic evolution is that
cultural evolution is inherently faster than genetic evolution.
Converging lines of evidence frommany disciplines indicate that
our psychological capacities for cultural learning evolved as an
This paper results from the Arthur M. Sackler Colloquium of the National Academy of
Sciences, In the Light of Evolution IV: The Human Condition, held December 1012,
2009, at the Arnold and Mabel Beckman Center of the National Academies of Sciences
and Engineering in Irvine, CA. The complete program and audio les of most presentations
are available on the NAS Web site at www.nasonline.org/SACKLER_Human_Condition.
Author contributions: P.J.R., R.B., and J.H. designed research, performed research, and
wrote the paper.
The authors declare no conict of interest.
This article is a PNAS Direct Submission.
1
To whom correspondence should be addressed. E-mail: pjricherson@ucdavis.edu.
This article contains supporting information online at www.pnas.org/cgi/content/full/
0914631107/DCSupplemental.
www.pnas.org/cgi/doi/10.1073/pnas.0914631107 PNAS | May 11, 2010 | vol. 107 | suppl. 2 | 89858992
adaptation to temporally and spatially variable environments (12,
13). By adding bias forces and the transmitted effects of individual
learning to random variation and natural selection, the cultural
system can more rapidly track changing environments than can
genes alone, albeit at some considerable cost in maintaining a large
brain to support the cultural system (3, 14). Fast change also leads
to large differences between neighboring societies, an important
consideration for the evolution of human sociality (1). Even the
most sophisticated social learners among other species, such as
chimpanzees, are poor social learners compared with young chil-
dren (15). Recently, empirical investigations of cultural trans-
mission and evolution have become common (e.g., 7, 1618) and
much work in linguistics (19, 20), applied psychology (21), and
many other social scientic and historical investigations give con-
vincing evidence of cultural evolution.
Cultures create novel environments that lead to new pressures
from natural or social selection on genes (1). [We include here the
effects of niche construction (22) insofar as modications of the
environment are rooted in culturally transmitted technology or
social institutions.] To some degree, human culture is like any
system of phenotypic exibility. It has evolved to respond to en-
vironmental variation, allowing genes to be spared natural selec-
tion. Many elements of the biology of complex organisms such as
humans act as mechanisms of phenotypic exibility (23). For ex-
ample, many developmental processes have an element of random
variation and selective retention. Nerve axons growprolically and
are pruned if they do not nd appropriate targets. Like other
systems for the inheritance of acquired variation, culture can play
an active role in evolution through what is known as the Baldwin
effect (24, 25). Systems for phenotypic exibility, if they are
adaptive, will generate phenotypes that tolerate small environ-
mental changes and small genetic departures from current optima.
Near-selective optima, mechanisms of phenotypic exibility, shel-
ter near-optimal genetic variants from selection. But away from
selective optima, phenotypic exibility has the opposite effect. By
making survival and reproduction possible in novel environments,
a system of phenotypic exibility can expose genes to selection.
Thus, presumably, the anatomically modern human populations
that left tropical Africa to invade temperate and periglacial envi-
ronments in Eurasia adapted rst to them using clothing, shelter,
and re, but later also evolved husky physiques and lighter skin
pigmentation adapted to cold temperatures and low light (26).
Genes and culture resemble a symbiosistwo inheritance
systems occupying the same physical body. The cultural partner
can create complex adaptations rapidly compared with the ge-
netic partner. As cultural adaptations became important, much
could be gained from imitating a seemingly successful idea or
practice. If people can judge what is successful, or who is suc-
cessful, new adaptive variation can rapidly spread through an
entire population, sometimes within one generation. This ability
might have been particularly important in glacial climates that
were extremely variable on timescales ranging from a generation
to a few tens of generations. Theoretical models suggest that
such variation should favor the evolution of a cognitively costly
system of cultural adaptation (13). When variation has smaller
amplitudes or longer timescales, selection causes genetic varia-
tion to track environmental changes at a lesser cost. When var-
iation is strong at timescales of a generation or less, individual
learning and other nontransmitted mechanisms for phenotypic
exibility will be favored by selection. The human genome and its
associated biology provide a large brain, anatomic modications
for speech, and no doubt a large number of other genetically
coded mechanisms that enable humans to host a fancy cultural
system (3). At the same time, complex cultural systems will tend
to adapt to genetically constrained cognitive capacities so as to
be learnable and useful. Cultural adaptation to constrained
cognition has recently been argued to be the case for language
acquisition (27) and reading (28).
Coevolutionists debate whether cultural evolution was largely
controlled by selection acting on genes or whether cultural evo-
lution often played the leading role during human evolution. For
example, Wilson (29) argues that epigenetic rules controlled
cultural evolution until the latest Pleistocene or Holocene. In
contrast, we have argued that cultural evolution has played a large
role in shaping human genes. For example, group selection on
cultural variation plausibly played a leading role in the evolution
of genes underpinning our unusual social systems, including co-
operative breeding and cooperation among distantly related
individuals (1, 30). Theory suggests that variation between groups
can more easily be created in the cultural than the genetic system,
and this prediction has some empirical support (18). Did natural
selection rst create capacities for culture for noncultural reasons
after which cultural evolution began, as Ayala (31) argues for
systems of morality, or did culture commonly play leading roles in
gene-culture coevolution, even in the evolution of the earliest
hominins? Perhaps human nature itself is substantially a product
of cultural evolution inuencing human genetic evolution by
a systematic, large-scale Baldwin effect.
Gene-Culture Coevolution in Hominin History
Wood (32) provides an outline of human evolution. Studies of
living apes (e.g., 33) suggest that culture has been at least a mi-
nor part of hominin capabilities since our last common ancestor
with chimpanzees. Culture-led gene-culture coevolution thus
potentially has a deep history in our lineage. Later, cultural
evolution led to innovations in technology that, for example,
made scavenging and hunting of meat productive. Ample meat
and fat in diets, together with cooking, would have supported the
evolution of larger, more expensive brains (3437), leading to
still-more sophisticated technology that eventually led to humans
becoming specialized hunters of big game during the last couple
of glacial cycles (38). After 11,500 years ago, as the highly vari-
able climates of the last ice age gave way to the much less vari-
able climates of the Holocene, plant resources began to be
exploited intensively in many parts of the world. Agriculture
progressively became the dominant subsistence system in most
parts of the world (39). At the same time, human social orga-
nization was revolutionized. Evidence reviewed below shows that
agricultural subsistence led to many genetic changes, but evi-
dence regarding older episodes of coevolution is still scanty.
The idea that cultural variation fell under group selection at the
scale of tribes is a modernization of a hypothesis rst proposed by
Darwin in the Descent of Man (40). Our last common ancestor
with the other apes presumably had a social system based on
dominance, with no provisioning of offspring beyond mothers
milk. Cooperative breeding seems to have been essential to pro-
vide food supplements to mothers and juveniles to support the
expansion of brains (41). In anatomically modern humans, at least
to judge by well-studied ethnographic examples, adult male
hunters produced a large surplus of meat and fat that was chan-
neled to women and children (36, 42). To reduce the risk of big-
game hunting, males cooperated in band-sized units including
several good hunters. Bands were exible units within a larger
ethnolinguistic tribe from which bands drew members, partly but
not entirely along kinship lines. As populations increased with the
evolution of plant-intensive foraging and agriculture, population
densities increased and social sophistication increased still fur-
ther, leading to formal political systems (advanced chiefdoms and
small states) by the Middle Holocene and to large states and
empires in the classical period (43). Somewhere along this tra-
jectory of increasing social sophistication, humans developed
a social psychology organized around culturally acquired social
rules (norms to psychologists, institutions to sociologists)
(44). People came to take on social identities that tied them-
emotionally to their social groups (45). We became exquisitely
sensitive to social boundaries symbolically marked by language,
8986 | www.pnas.org/cgi/doi/10.1073/pnas.0914631107 Richerson et al.
dress, ritual, and other stylistic differences between us and
them (ref. 8, chap. 9, 464748).
The paleoanthropological record is seriously decient, as fossil
records always are. Many forms of technology are very rarely
preserved, including those made of wood, organic bers, and
leather. Usage wear on stone tools suggests that they were often
used to make such products. Very rare nds, such as three
aerodynamically sophisticated wooden javelins from an anaero-
bic deposit in Germany dating to 400 kya (49), suggest that re-
lying entirely on stone artifacts to deduce the technical
sophistication of archaic humans is potentially misleading. In-
ferring the sizes of human populations from the paleoanthro-
pological record is also difcult. Demography is important
because cumulative cultural sophistication advances further and
faster in large interconnected than in small isolated populations
(50, 51). Thus, human populations with identical spectra of in-
dividual cognitive ability can produce sophisticated or simple
tools, depending upon effective population size. Exogenous
controls on human populations from climate and competition
with other species may be important. For example, in southern
Africa between 70 and 80 kya, two short episodes with more
sophisticated artifacts punctuate a long record with the less so-
phisticated Middle Paleolithic artifacts, perhaps because of
population boom-and-bust events (52, 53). Immediately after
anatomically modern humans left Africa, most populations seem
to have been making Middle Paleolithic artifacts but, a short
time later, the Upper Paleolithic peoples of western Eurasia
made sophisticated tools and produced a large corpus of art (54)
of a complexity only observed in some of the most complex
ethnographically and historically known foraging populations.
Thus, the four most obvious indices of human cognitive
complexity, brain size, ability to colonize a wide range of envi-
ronments, stone tool complexity, and artistic productions, are
only very imperfectly correlated, for reasons that remain enig-
matic. Inferences about past behavior and social organization are
necessarily based on slim evidence. Some authors argue that
even quite ancient hominins had modern behavior (55). For
example, Lovejoy suggests that the reduced canines of Ardipi-
thecus ramidus, a form thought to be close to the last common
ancestor with the other apes, indicate important social innova-
tions very early in our lineage (56). At the other extreme, Klein
(ref. 57, pp. 652653) argues that at least one major social or
cognitive modernization must have precipitated the exodus of
anatomically modern humans out of Africa quite late in our
evolutionary history. Both of these claims are controversial. Al-
though the hypothesis that fast cultural evolution should have
driven the gene-culture coevolutionary process is plausible on
theoretical grounds, the fact is that the large brain of anatomi-
cally modern humans predates the Upper Paleolithic cultural
system by perhaps 150 kya. Perhaps chronically low population
densities prevented the cumulative cultural evolution of highly
complex tools and symbolic behavior that characterize the Upper
Paleolithic and Later Stone Age (51). Favorable circumstances
that allowed more substantial populations, particularly in west-
ern Eurasia after 40 kya and more generally in the Holocene,
may have allowed anatomically modern humans to create highly
elaborated cultures much along the line of Ayalas (31) hy-
pothesis about morality. Our hypothesis that culture was gener-
ally the leading rather than the lagging variable in the
coevolutionary system may not always (or ever) be correct, even
late in hominin evolution. Genomic data promise to have a large
impact by shedding light on questions that are difcult to resolve
with traditional methods.
New Genomic Tools
Whereas paleoanthropologists will make slow progress in solving
the many riddles hinted at in the preceding section, the genomics
revolution, made possible by the rapidly falling cost of se-
quencing genomes, is providing important new tools. These
methods promise two important contributions. First, they al-
ready help us to better understand paleodemography (58). Sec-
ond, genomic methods can be used to estimate where and when
selection has occurred in the human genome.
Mitochondria and autosomal lineage coalescence times record
some evidence of past genetic bottlenecks. When population
sizes are small, genetic diversity is lost by drift. If a population
increases suddenly, as the hominin population did when ana-
tomically modern humans expanded out of Africa, then a larger
number of genes will have coalescence times indicating the time
when the human population became large enough to sustain
higher diversity. Coalescence times are older for autosomes than
for mitochondria or Y chromosomes in part because the effec-
tive population size for diploid autosomes is four times the size
of the population of maternally transmitted haploid mitochon-
dria or paternally transmitted Y chromosomes (59).
Studies of the mitochondrial and autosomal genomes have
given an interesting picture of the demographic expansion out of
Africa. A succession of population bottlenecks caused decreasing
genetic diversity farther away from our ancestral African
homeland (6064). The populations most distant from one an-
other, measured by the length of the most likely migration path
from Africa, are most distant from one another genetically.
Thus, the picture of the genetic architecture of human pop-
ulations derived from molecular methods bears a strong re-
semblance to that derived from classical human genetics (65).
Africans maintain the most genetic diversity, and the most dis-
tant migrants out of Africa retain the least due to successive
bottlenecks. Selective sweeps and genetic drift have similar
effects on the genome, so the most efcient estimation methods
for dating selective sweeps are those which use selectively neutral
variation to estimate population sizes and control for the effects
of drift. The effects of selection on potentially nonneutral vari-
ation are then apparent as departures from expectations based
on a neutral model (66, 67). To this point, limitations in the size
and nature of the samples of sequenced human DNA do not
allow high condence in either the population or selection
reconstructions. The continuing fall in the costs of sequencing
will increase sample sizes and coverage, and statistical methods
will most likely continue to improve as well.
Sabeti et al. (68) review the methods for detecting the action
of selection on the genome on various timescales. On the longest
timescales, selection is evidenced by functionally signicant dif-
ferences between species. For example, the FOXP2 gene has two
functionally signicant differences between humans and chim-
panzees. Preliminary sequences of Neandertal DNA suggest that
we share these two changes with that species, thus placing the
evolution of these changes before the separation of the two
species several hundred thousand years ago (but see a discussion
of problems with this interpretation below). Selective changes
will show an excess of changes at sites that change amino acids of
proteins compared with synonymous sites that do not. At shorter
timescales, less than 250 kya, positive selection leaves a signa-
ture of reduced diversity in genes linked to the target of the
selective sweep due to hitchhiking. Mutation and drift eventually
restore this diversity, but in the meantime an excess of rare
alleles in the linked region provides an estimate of the timing of
the selective sweep. At time scales < 80 kya, the linked region
will contain an excess of derived alleles that have hitchhiked to
high frequency along with the allele that was the target of se-
lection. As human populations left Africa and became exposed
to divergent selection in different environments and cultures,
different alleles will be swept to high frequency in different
populations (< 60 kya). Even if selection pressures are the
same in different populations, and an allele with the same
function is selected in different populations, the alleles in the
different populations are likely to contain neutral differences in
Richerson et al. PNAS | May 11, 2010 | vol. 107 | suppl. 2 | 8987
sequence. The LCT regulatory gene down-regulates the secre-
tion of lactase postweaning in most human populations. In
western Eurasian and African dairying populations the gene is
rendered nonfunctional, so that adults continue to secrete lac-
tase and to benet from lactose. Sequencing of the adult secre-
tion variants of LCT from western Eurasia and Africa revealed
that they were dysfunctional in different ways (69). Finally, at
time scales < 30 kya, the linked hitchhiking region around the
selected allele will not have been subject to recombination for
a time-dependent length of sequence. The whole haplotype will
be monomorphic for a certain distance. Thus, the LCT gene,
which evolved after the evolution of dairying 5,000 years ago, is
associated with a long monomorphic haplotype. Recombination
reduces linkage disequilibrium around the selected allele over
time, providing a rough estimate of the time of the sweep.
Akey (70) has reviewed the promise and pitfalls of DNA se-
quence methods based on 21 genome-wide scans for alleles un-
der selection. To assess the reliability of these methods, Akey
compared eight genome-wide scan studies using the Hapmap
and Perlgen databases. The eight studies reported a total of
5,110 distinct regions under selection, but only 14.1% were
identied in two or more studies and 2.5% in four or more.
Nevertheless, he nds grounds for cautious optimism. First,
many of the genes that occur in multiple studies have already
been rmly identied as under selection, such as the LCT gene.
Second, many of the genes under selection exhibit geographical
differences. Because humans have recently spread from a tropi-
cal African homeland to the rest of the world, it is plausible that
many genes have experienced divergent selection in the last
60,000 years. Evolution during this period is relatively easy to
detect and many alleles under recent selection should be adap-
tations to the new local environments into which humans were
dispersing. Signicant issues remain. Some reect the small and
possibly nonrepresentative sample of genomes available for
study. This defect will be remedied fairly rapidly. Statistical
methods for detecting selection are also likely to improve dra-
matically (71). A deeper difculty is the lack of understanding
from genomics alone about the phenotypic effects of the genes
that selection has targeted. In the case of genes with strong and
direct phenotypic effects, such as LCT, HBB (the sickle cell
gene), other genes coding for resistance to malarias, skin pig-
mentation genes, and a few others, a functional understanding of
the genes preceded genomic analysis, which has added only
wrinkles to the classic stories. Presumably, many of the genes
under selection are quantitative trait loci in which selection for
a given phenotype will exert weak selection at many loci. Func-
tional annotations for genes that are transcribed into proteins
give only general hints about the function of the particular alleles
that have been selected in the human lineage. We do not seem to
have any substitute for functional studies targeted on sequences
that have apparently undergone recent selection to understand
why they might have come under selection. To advance rapidly
on a broad front will require the same sorts of high-throughput
methods that have revolutionized genomics also be applied to
the expression of genes during development, on the model of
ChIP-on-chip technology, which is still in its infancy as far as
vertebrate epigenomics is concerned.
Studies of the FOXP2 gene provide a cautionary tale, exempli-
fying our still-primitive understanding of the connection between
genotypes and phenotypes (72, 73). This gene, coding for a regu-
latory protein, has apparently been under strong selection since
the last common ancestor with the other apes. Two amino acid
substitutions have taken place in the hominin lineage. Early
reports from a study of language decits in a family with a rare
FOXP2 mutant suggested to some that it is a grammar gene.
However, it turns out to be a highly conserved gene that is
expressed in a wide variety of tissues during vertebrate de-
velopment. In the brain, a ChIP study shows that it down-regulates
CNTNAP2, the gene encoding contactin-associated protein-like 2,
a member of the neurexin superfamily. This gene is involved with
cell recognition and cell adhesion, playing a role in nervous system
development, including in the human frontal cortex during mid-
development. Hence, it is expressed in tissues that may well relate
to language abilities. However, other studies identied several
hundred other potential targets of FOXP2 as though it plays a role
in many regulatory circuits during development.
The timing of the evolution of the common human FOXP2
allele has also proven perplexing. The region near the sub-
stitutions in the derived human gene contains a high frequency of
derived neutral variants that have not been disrupted by re-
combination, suggesting that the second of the two human sub-
stitutions on the gene must have taken place in the last 130 kya
(73). On the other hand, Krause et al. (74) sequenced Nean-
dertal DNA and recovered the same genotype as modern
humans, implying that the modern human allele evolved more
than 300 kya. Several hypotheses have been proposed to explain
this puzzle. They include (i) laboratory artifacts, (ii) in-
trogression between Neandertals and anatomically modern
humans (75), and (iii) the possibility that the two amino acid
substitutions are ancient, and that the linkage disequilibrium
observed in modern humans arose from recent selection on
a nearby gene rather than on FOXP2 itself (73, 76). Thus, al-
though the promise of genomics and related high-throughput
techniques to study human evolution is high, human biology,
evolutionary history, and extant population structure are all in-
timidatingly complex. Not every problem will be quickly solved,
and many analytical improvements are needed.
The External Selective Environment
The role of culture in adapting to temporal and spatial environ-
mental variability has long been an important theme in gene-
culture coevolution theory (7779). Environmental change over
the course of hominin evolution has been substantial. Climate
variation correlated with variations in Earths orbit has pro-
gressively increased and shifted from the dominance of the 23-kyr
(precession) cycle in the Miocene and Early Pliocene to the
dominance of the 41-kyr (tilt) cycle from the Middle Pliocene
through the Early Pleistocene, and nally to the dominance of the
100-kyr cycle (eccentricity) during the Middle and Late Pleisto-
cene. The Middle Pliocene shift roughly correlates with the ap-
pearance of our genus, Homo, and the evolution of progressively
larger-brained and technically more sophisticated humans occurs
after the mid-Pleistocene shift (80). Variation on the orbital
timescales (900+ human generations) probably has little direct
impact on the gene-culture system. The higher-frequency com-
ponents of climate variation, which are perhaps correlated with
the lower-frequency orbital scale uctuations, are likely to be
much more important. High-resolution ice cores from Greenland
rst revealed that high-frequency, high-amplitude submillennial
and millennial variation (1100 human generations) occurred
during the last ice age (81). Long high-resolution ocean cores
suggest that the tempo of this variation has increased over the last
four cycles (82). High-resolution paleoclimate data for the whole
course of hominin evolution would be very interesting but do not
yet exist.
The models of gene-culture coevolution described above,
which predate the high-resolution paleoclimate data, suggest
that a cognitive capacity to support a costly system for cultural
transmission and evolution is favored by just such high-amplitude
millennial and submillenial scale variations as occurred during at
least the last four glacial cycles. Without such variation, genes
and nontransmitted phenotypic exibility are sufcient to allow
a population to adapt to variation (ref. 3, pp. 125131, 79)
without the need for the faster-tracking but expensive cultural
system. The paleoclimate data, as they currently stand, are
consistent with the hypothesis that the evolution of human cul-
8988 | www.pnas.org/cgi/doi/10.1073/pnas.0914631107 Richerson et al.
ture has been in response to increasing environmental variation
over time. We know that brain-size increase is not unique to
humans. Many mammalian lineages show increased brain size in
the last couple of million years (83). Increases in mammalian
brain size averaged over many lineages might be taken as
a paleoclimate index of the amount of high-frequency environ-
mental variation, on the grounds that costly nervous tissue would
not evolve unless useful for adapting to high-frequency envi-
ronmental change by individual learning and simpler forms of
social learning (34, 84, 85).
Current Evidence and Problems to Solve
In this section, we outline the still-modest evidence that culture-
led gene-culture coevolution has been the dominant mode of
human evolution, perhaps reaching back to the divergence of
hominins from our last common ancestor with the other apes.
The modest culture of chimpanzees and many other organisms
(8688) might also induce important gene-culture coevolution by
a cultural Baldwin effect.
The best evidence about gene-culture coevolution comes from
the present and immediate past (89). Estimating the current
strength and direction of selection is a classic topic in evolu-
tionary biology (90), and social scientists have conducted similar
studies (91, 92). The environmental, genetic, and cultural data
are rather good for the last 10 millennia. However, some of the
most interesting questions come from deeper history, where all
three kinds of investigations meet limits. Ancient ecosystems and
their variation are hard to reconstruct (93), evidence of distant
past selection is less precise than for recent selection, and the
number of fossils and artifacts discovered and their condition
declines with time (e.g., 94). The hope is that evolutionary
genomics and related functional studies will provide a powerful
third source of data to complement paleoenvironmental and
paleoanthropological data. The way forward will be to make
optimal use of all three forms of data, each with inevitable lim-
itations, in evaluating hypotheses about our evolution.
Current Selection. Most but not all contemporary human pop-
ulations have experienced rapid and dramatic cultural change in
recent times due to economic development and the globalization
of culture. Diseases and domesticates from all around the world
have been introduced to climatically compatible regions. Large
populations of mixed-race people have emerged. Many pop-
ulations have reduced exposure to infectious diseases. Some
populations have become so wealthy that consumption of food
leads to diseases of nutritional excess rather than diseases of
nutritional deciency. In the past two centuries, beginning in
Europe, an increasing number of societies have become highly
urbanized. Kin have become less important in social networks in
urban societies, leading to a host of tness-related changes in-
cluding demographic transitions and increasing tolerance for
lifestyles that do not result in reproduction (95). Kin-dense social
networks arguably support norms that encourage reproduction in
a society because kin selection will have favored kin taking more
interest in the reproduction of kin than in the reproduction of
nonkin friends.
These changes all seem likely to generate measurable selection
on genes. Some of these genetic changes are likely to result from
relaxed selection, for example due to the reduced importance of
infectious disease and nutritional deciency in many populations.
Some are likely to result from positive selection for resistance to
new environments. For example, modern urban environments are
often hygienically cleaned, apparently leading to the IgE com-
ponent of the immune system to respond to inappropriate targets
such as ones own tissue or harmless pollens (96, 97). Some of
these diseases, like asthma, have appreciable death rates among
children and young adults. A number of genes that might be
targets of selection are known to be involved in asthma.
Some of the complexities of gene-culture coevolution can be
illustrated by the impact of the demographic transition on ge-
netic and cultural evolution. Whereas most of us celebrate the
modern steep drop in fertility from the point of view of mod-
erating anthropogenic climate change and similar problems, the
rst-order effect of natural selection is to favor the efcient
conversion of resources into offspring. Thus, we might expect to
see current selection favoring more pronatalist behavior in
postdemographic transition societies. On the genetic side,
a study of the heritability of fertility in Danish twins showed that
the heritability of fertility was negligible in predemographic
transition times but has become appreciable in later cohorts (98,
99). Formerly, pronatalist culture, which must have been the
norm in most times and places throughout our evolutionary
history, would have effectively encouraged most people to re-
produce efciently, despite minor genetic variation that might
have led some people not to reproduce. A drastic fall in average
fertility has likely caused variation that was once neutral, or
nearly so, to have a much stronger effect on phenotypes. Two
studies report that life-history characteristics are currently
responding to selection (100, 101). Women seem to be under
selection to enter menarche earlier, have earlier rst births, and
to reach menopause later. They seem to sacrice height in the
process of earlier reproduction. As to mechanism, earlier rst
births may simply result from earlier menarche, exposing more
impulsive teenagers to risk of pregnancy.
Stearns and coauthors used the Framingham Heart Study to
estimate the effects on lifetime reproductive success of traits
measured in that study (102). Together with estimates of herit-
abilities of traits, they estimated selection strength on these
traits. Women are under measurable selection for shorter but
heavier bodies, earlier reproduction but also delayed meno-
pause, as in the studies described just above, and lower blood
pressure and lower cholesterol. The latter two traits suggest se-
lection to adapt to the sedentary lifestyles and rich diets in the
contemporary developed world.
Culture is also under selection to increase birth rates. Some
subcultures, such as Old Order Anabaptists, have proven quite
resistant to cultural modernization and have continued to re-
produce at natural fertility levels (7 children per woman).
Anabaptist populations are apparently growing very rapidly (103,
104). Hout et al. (92) estimated the selective effects of other
religious beliefs. The main effect in the United States seems to
be that religious people have about twice as many children as the
unchurched; differences among many denominations are other-
wise modest. At the global level, religion is currently spreading
faster than secularism because religious people are having more
children (105). Sociologists of religion have argued that early
Christianity spread in part by demographic increase in the Ro-
man Empire because of its pronatalist proscriptions and pre-
scriptions (106).
Selection in the Holocene. About 11,500 years ago the climate sta-
bilized, beginning the current relatively invariant, warm, and wet
interglacial. Over the next few thousand years, most human pop-
ulations adopted some form of agricultural subsistence (39). Late
Pleistocene humans appear to have depended disproportionately
on game animals for subsistence (107). Thus, switching to a diet
rich in plant carbohydrates confronted people with dietary chal-
lenges (108). Plant-rich diets also meant that human numbers
could increase, leading to the acquisition of newepidemic diseases,
often from domestic animals (109). Dense populations also led
to the cultural evolution of new forms of social organization to
replace the smaller-scale egalitarian societies that typify many
hunter-gathers. Large social systems arose with hierarchically or-
ganized authority and an elaborate division of labor.
The evidence suggests that many new genes came under se-
lection in the Early and Middle Holocene (110). Some of these
Richerson et al. PNAS | May 11, 2010 | vol. 107 | suppl. 2 | 8989
are familiar human polymorphisms already discussed, such as the
HBB sickle cell gene, the G6PD malaria protection gene, and the
LCT adult lactose secretion gene. Other interesting genes in-
clude amylase copy-number polymorphisms. Populations with
a recent history of diets rich in starch have more copies of the
gene coding for amylase (111). The functional annotations of
genes identied in large-scale scans (e.g., 68) ag many as po-
tentially of signicance in disease resistance or dietary adapta-
tions. As the vast task of identifying the functions of many genes
proceeds, we anticipate many similar cases to emerge (112114).
The category that will be controversial is genes related to
behavior. The transformation of human social systems in the
Holocene is every bit as dramatic as the transition in diet and
disease exposure. Should we expect that many genes adapted to
more complex and more hierarchical societies have arisen in the
Holocene? Cochran and Harpending (115) have suggested that
the Ashkenazi Jews have high intelligence, and a concentration
of genetic diseases with neurological symptoms, due to their
Medieval specialization in the businesses of banking and long-
distance trade, and later in various managerial occupations.
These jobs, emphasizing intellectual skills, generated selection
for high IQ. Jews of that time were also relatively genetically
isolated. Some of these genes are perhaps overdominant, leading
to neurological pathologies when homozygous. One might
imagine that the human division of labor is extensively supported
by genetic specializations favoring different occupations. As
cultures developed a larger number of economic and social roles,
human genetic diversity might have increased to diversify human
capabilities and inclinations. The honeybee division of labor is
supported by queens mating multiply and so diversifying the
genes of workers, whose differing genotypes are better at dif-
ferent tasks (116). This hypothesis suggests that genes controlling
such things as personality should be more variable in populations
that have long had a history of an extensive division of labor.
On the other hand, culture is a tremendous force for gener-
ating behavioral variation independently of genetic variation.
Thus, human genetic variation for behavioral traits may be large
because cultural variation shelters much genetic variation from
selection. Literacy rates in societies with good education systems
can approach 100% despite the fact that reading is not some-
thing human brains evolved to do. Rather, cultures evolved
writing systems that take advantage of parts of the brain evolved
to do quite different things (28). Cultures nd ways to nesse
disabilities so that the blind and dyslexic can learn to read. The
idea that traits with high heritabilities such as IQ are unaffected
by the cultural environment is falsied by the rapid secular in-
crease in IQ in many developed countries during the 20th cen-
tury (117), and by the fact that IQ is much less heritable among
populations with lower socioeconomic status (118). Likewise, IQ
is correlated across countries with stage of modernization (119).
The amount and quality of education seem to explain most of the
variation in IQ between groups and over time within groups
(120). Botticini and Eckstein (121) argue that a tradition of
education and literacy accounts for Jews entering jobs requiring
high intellectual skills. Of course, this hypothesis and Cochran
and Harpendings are not mutually exclusive. To what extent are
the genes that underlie behavioral variation in humans evolving
mostly by drift and mutation because they are protected from
selection by culture, and to what extent have they been under
frequency-dependent selection to support the division of labor in
complex societies?
Selection in the Plio-Pleistocene. Humans emerged from the Late
Pleistocene with a highly advanced capacity for culture and
promptly evolved agricultural subsistence systems that radically
altered human environments. The strong coevolutionary impact
of cultural changes on genes in the Holocene is not surprising.
But how far back into hominin history was this mode of co-
evolution important? Theory points to the speed of cultural
evolution compared with genetic evolution. Even rudimentary
culture capacities could support appreciable amounts of culture-
driven gene-culture coevolution. This idea is difcult to test in
humans given the limitations of the current record mentioned in
the introduction to this section. Certain aspects of the record are
now reasonably well understood, namely skeletons and stone
tools. Genomic clocks can potentially be calibrated by matching
the evolution of genes directly affecting skeletons and abilities to
make stone tools to the paleoanthropological record. If genomic
analysis can provide at least rough dates for when traits and
capacities that are more poorly represented in the paleoan-
thropological record evolved, it will provide an important new
source of information about how the coevolutionary process
works. The logic of the argument can be illustrated by the ref-
utation of an early coevolutionary hypothesis proposed by
Sherwood Washburn (122). Washburn speculated that a co-
evolutionary process was set up by the development of traditions
of making simple stone tools. The use of tools created environ-
ments that favored the specialization of hands for toolmaking,
leading toward upright posture. As hands became more special-
ized for toolmaking, selection would favor larger brains, including
improved manual dexterity in ne manipulations, that would
underpin more complex tool traditions. This hypothesis is not
correct, at least not in the simple form that Washburn proposed.
Australopithecines were bipedal for several million years without
any evidence of brain-size increase or tool use. Many plausible
scenarios about human evolution in the Plio-Pleistocene have
been advanced. Most of these are hard to test using skeletal and
stone tool evidence alone. In SI Text, we illustrate how genomic
data might help improve our understanding of hominin evolution
in the Plio-Pleistocene.
Conclusions
Genomics has already made quite substantial contributions to
our understanding of human evolution, beginning with the use of
mitochondrial DNA variation to understand the timing of events
in recent human evolution and to provide a window into human
paleodemography, including past population sizes and migration
patterns. The use of linkage disequilibrium to identify genes
under recent selection suggests a massive Holocene wave of
genetic change initiated by the cultural evolution of agricultural
subsistence. Even here, our lack of knowledge of the functional
signicance of most of the alleles that have been under selection
hides most of the details from us. As regards Plio-Pleistocene
gene-culture coevolution, we are still at the very beginning of an
understanding. In addition to a poor understanding of gene
function, it is not clear how much information gene sequences
contain about the timing of their selective history. Tools besides
simple linkage disequilibrium suitable for deeper time will be
required if genomics is to make a major contribution to resolving
the many puzzles of the paleoanthropological record. We expect
continued rapid progress.
ACKNOWLEDGMENTS. Many thanks to Francisco Ayala and John Avise for
organizing such an interesting conference and to our fellow presenters for
enlightening papers and discussions.
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