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12
Gene–Culture Coevolution in the Age of Genomics

PETER J. RICHERSON,*§ ROBERT BOYD, AND JOSEPH HENRICH

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 environments created by cultural innovations. Some changed in response to the development of agricultural subsistence systems in the Early and Middle Holocene, including alleles coding for adaptations to diets rich in plant starch (e.g., amylase copy number) and for adaptations to epidemic diseases that evolved as human populations expanded (e.g., sickle cell and G6PD deficiency alleles that provide protection against malaria). Large-scale scans using patterns of linkage disequilibrium to detect recent selection suggest that many more genes evolved in response to agriculture. 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. Also unknown is the role of paleoenvironmental change in regulating the tempo of hominin evolution. Although the full extent of culture-driven gene–culture coevolution is thus far unknown for the deeper history of

*

Department of Environmental Science and Policy, University of California, Davis, CA 95616;

Department of Anthropology, University of California, Los Angeles, CA 90095; and

Departments of Psychology and Economics, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.

§

To whom correspondence should be addressed. E-mail: pjricherson@ucdavis.edu.



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12 Gene–Culture Coevolution in the Age of Genomics PeTer J. riCherson,*§ roBerT BoyD,† AnD JosePh henriCh‡ 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 envi- ronments 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 environments created by cultural innova - tions. some changed in response to the development of agricultural subsistence systems in the early and Middle holocene, including alleles coding for adaptations to diets rich in plant starch (e.g., amylase copy number) and for adaptations to epidemic diseases that evolved as human populations expanded (e.g., sickle cell and G6PD deficiency alleles that provide protection against malaria). large-scale scans using patterns of linkage disequilibrium to detect recent selection suggest that many more genes evolved in response to agriculture. 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. Also unknown is the role of paleoenvironmental change in regulating the tempo of hominin evolution. Although the full extent of culture-driven gene–culture coevolution is thus far unknown for the deeper history of *Department of environmental science and Policy, University of California, Davis, CA 95616; †Department of Anthropology, University of California, los Angeles, CA 90095; and ‡Depart- ments of Psychology and economics, University of British Columbia, vancouver, BC v6T 1Z4, Canada. §To whom correspondence should be addressed. e-mail: pjricherson@ucdavis.edu. 

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 / Peter J. Richerson et al. 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 hominin evolutionary history. T he human cultural system supports the cumulative evolution of complex adaptations to local, often ephemeral environments. 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 con- stitute one of the world’s most impressive adaptive radiations. We have occupied virtually every habitat on earth by using technology and social organization to generate thousands of socioeconomic systems (henrich and Mcelreath, 2003; richerson and Boyd, 2005). CULTURAL EVOLUTION AND GENE–CULTURE COEVOLUTION Culture has many definitions, 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 (Boyd and richerson, 1985). Transmission fidelity is often sufficiently high for culture to act as an inheritance system (henrich and Boyd, 2002). We commonly observe that the ideas, practices, skills, attitudes, norms, art styles, technol- ogy, 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 knowledge of the differences between elizabethan and modern english. Culture is thus a system of descent with modification. 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 fields as diverse as population genetics, epide - miology, ecology, game theory, and stochastic processes (Cavalli-sforza and Feldman, 1981; Boyd and richerson, 1985). Those familiar with genetic evolution may be aided by considering some of the similarities and differences between genetic and cultural

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Gene–Culture Coevolution in the Age of Genomics /  evolution. Key differences include the nature of forces that act on cul- tural 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 individual’s life chances as a consequence of using different cultural variants (natural selection). other forces on cultural evolution are distinc- tive 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 observe. Assuming their choices are not random, this creates a variety of bias forces that can be defined by how the choices are made (richerson et al., 2003). humans also selectively transmit variants that they have learned to their offspring and to others. We call such psychological processes “decision-making forces.” Parent-offspring transmission dominates much (although not all) genetic transmission. in contrast, evidence on transmission patterns from a variety of sources indicates 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 (hewlett and Cavalli-sforza, 1986; henrich and henrich, 2007; Mcelreath et al., 2008). 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 (rogers, 1995; richerson and Boyd, 2005). For example, when American sweet potatoes tolerant of cool weather became available to the peoples of highland new Guinea a few centuries ago, the new crop set off a population explosion and a spurt of parallel social and economic innovations in a number of highland societies (Wiessner and Tumu, 1998). 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 from many disciplines indicate that our psychological capacities for cultural learning evolved as an adaptation to temporally and spatially variable environments (richerson et al., 2005; herrmann et al., 2007). By adding bias forces and the transmitted effects of individual learning to random variation and natural selection, the cul- tural system can more rapidly track changing environments than can

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 / Peter J. Richerson et al. genes alone, albeit at some considerable cost in maintaining a large brain to support the cultural system (Boyd and richerson, 1985; richerson and Boyd, 2001). Fast change also leads to large differences between neigh- boring societies, an important consideration for the evolution of human sociality (richerson and Boyd, 2005). even the most sophisticated social learners among other species, such as chimpanzees, are poor social learners compared with young children (Whiten et al., 2009). recently, empirical investigations of cultural transmission and evolution have become com - mon (e.g., Mesoudi, 2007; efferson et al., 2008; Mcelreath et al., 2008; Bell et al., 2009) and much work in linguistics (labov, 2001; Tomasello, 2008), applied psychology (rogers and shoemaker, 1971), and many other social scientific and historical investigations give convincing evidence of cultural evolution. Cultures create novel environments that lead to new pressures from natural or social selection on genes (richerson and Boyd, 2005). [We include here the effects of niche construction (odling-smee et al., 2003) insofar as modifications of the environment are rooted in culturally transmitted tech- nology or social institutions.] To some degree, human culture is like any system of phenotypic flexibility. it has evolved to respond to environmental variation, allowing genes to be spared natural selection. Many elements of the biology of complex organisms such as humans act as mechanisms of phenotypic flexibility (Kirschner and Gerhart, 1998). For example, many developmental processes have an element of random variation and selec- tive retention. nerve axons grow prolifically and are pruned if they do not find 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 (Baldwin, 1896; Ghalambor et al., 2007). systems for phenotypic flexibility, if they are adaptive, will generate phenotypes that tolerate small environmental changes and small genetic departures from current optima. near selective optima, mechanisms of phenotypic flexibility shelter near-optimal genetic variants from selection. But away from selective optima, phenotypic flexibility has the opposite effect. By making survival and reproduction possible in novel environ- ments, a system of phenotypic flexibility can expose genes to selection. Thus, presumably, the anatomically modern human populations that left tropical Africa to invade temperate and periglacial environments in eurasia adapted first to them using clothing, shelter, and fire, but later also evolved husky physiques and lighter skin pigmentation adapted to cold tempera- tures and low light (Jablonski and Chaplin, Chapter 9, this volume). Genes and culture resemble a symbiosis—two inheritance systems occupying the same physical body. The cultural partner can create complex adaptations rapidly compared with the genetic partner. As cultural adapta- tions became important, much could be gained from imitating a seemingly

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Gene–Culture Coevolution in the Age of Genomics /  successful idea or practice. if people can judge what is successful, or who is successful, 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. Theo- retical models suggest that such variation should favor the evolution of a cognitively costly system of cultural adaptation (richerson et al., 2005). When variation has smaller amplitudes or longer timescales, selection causes genetic variation to track environmental changes at a lesser cost. When variation is strong at timescales of a generation or less, individual learning and other nontransmitted mechanisms for phenotypic flexibility will be favored by selection. The human genome and its associated biology provide a large brain, anatomic modifications for speech, and no doubt a large number of other genetically coded mechanisms that enable humans to host a fancy cultural system (Boyd and richerson, 1985). 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 (Kirby et al., 2007) and reading (Dehaene, 2009). Coevolutionists debate whether cultural evolution was largely con- trolled by selection acting on genes or whether cultural evolution often played the leading role during human evolution. For example, Wilson (1998) 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 cooperative breeding and cooperation among distantly related individuals (henrich, 2004a; richerson and Boyd, 2005). Theory suggests that varia- tion between groups can more easily be created in the cultural than the genetic system, and this prediction has some empirical support (Bell et al., 2009). Did natural selection first create capacities for culture for non - cultural reasons after which cultural evolution began, as Ayala (Chapter 16, this volume) 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 influencing human genetic evolution by a systematic, large-scale Baldwin effect. GENE–CULTURE COEVOLUTION IN HOMININ HISTORY Wood (Chapter 1, this volume) provides an outline of human evolu- tion. studies of living apes [e.g., Whiten et al. (1999)] suggest that culture

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 / Peter J. Richerson et al. has been at least a minor 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 (Aiello and Wheeler, 1995; Gurven and hill, 2009; hill and hurtado, 2009; Wrangham, 2009), leading to still-more sophisticated technology that eventually led to humans becoming specialized hunters of big game dur- ing the last couple of glacial cycles (stiner, 2002). After 11,500 years ago, as the highly variable climates of the last ice age gave way to the much less variable 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 (richerson et al., 2001). At the same time, human social organization was revolutionized. evidence reviewed below shows that agricultural subsistence led to many genetic changes, but evidence 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 first proposed by Darwin in the Descent of Man (richerson and Boyd, 2004). our last common ancestor with the other apes presumably had a social system based on dominance, with no provisioning of offspring beyond mother’s milk. Cooperative breeding seems to have been essential to provide food supplements to mothers and juveniles to support the expansion of brains (Burkart et al., 2009). in ana- tomically modern humans, at least to judge by well-studied ethnographic examples, adult male hunters produced a large surplus of meat and fat that was channeled to women and children (Kaplan et al., 2000; hill and hurtado, 2009). To reduce the risk of big-game hunting, males cooperated in band-sized units including several good hunters. Bands were flexible units within a larger ethnolinguistic tribe from which bands drew mem- bers, 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 further, leading to formal political systems (advanced chiefdoms and small states) by the Middle holocene and to large states and empires in the classical period (Johnson and earle, 2000). somewhere along this trajectory of increasing social sophistication, humans developed a social psychology organized around culturally acquired social rules (“norms” to psychologists, “institu- tions” to sociologists) (richerson and Boyd, 2008). People came to take on social identities that tied them emotionally to their social groups (haslam, 2001). We became exquisitely sensitive to social boundaries symbolically marked by language, dress, ritual, and other stylistic differences between

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Gene–Culture Coevolution in the Age of Genomics /  “us” and “them” (Mcelreath et al., 2003; henrich and henrich, 2007, chap. 9, pp. 175–178; Kinzler et al., 2007; shutts et al., 2009). The paleoanthropological record is seriously deficient, as fossil records always are. Many forms of technology are very rarely preserved, includ - ing those made of wood, organic fibers, and leather. Usage wear on stone tools suggests that they were often used to make such products. very rare finds, such as three aerodynamically sophisticated wooden javelins from an anaerobic deposit in Germany dating to 400 kya (Thieme, 1997), suggest that relying entirely on stone artifacts to deduce the technical sophistication of archaic humans is potentially misleading. inferring the sizes of human populations from the paleoanthropological record is also difficult. Demography is important because cumulative cultural sophis - tication advances further and faster in large interconnected than in small isolated populations (henrich, 2004b; Powell et al., 2009). Thus, human populations with identical spectra of individual cognitive ability can pro - duce sophisticated or simple tools, depending upon effective population size. exogenous controls on human populations from climate and com- petition with other species may be important. For example, in southern Africa between 70 and 80 kya, two short episodes with more sophisti - cated artifacts punctuate a long record with the less sophisticated Middle Paleolithic artifacts, perhaps because of population boom-and-bust events (Jacobs et al., 2008; richerson et al., 2009). 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 (Foley and lahr, 1997) 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 environments, stone tool complexity, and artistic productions, are only very imperfectly correlated, for reasons that remain enigmatic. inferences about past behavior and social organization are necessarily based on slim evidence. some authors argue that even quite ancient hominins had modern behavior (isaac, 1981). For example, lovejoy suggests that the reduced canines of Ardipithecus ramidus, a form thought to be close to the last common ancestor with the other apes, indicate important social innovations very early in our lineage (lovejoy, 2009). At the other extreme, Klein (2009, pp. 652–653) 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 contro- versial. Although the hypothesis that fast cultural evolution should have driven the gene–culture coevolutionary process is plausible on theoretical

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 / Peter J. Richerson et al. grounds, the fact is that the large brain of anatomically 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 (Powell et al., 2009). Favorable circumstances that allowed more substantial populations, particularly in western eurasia after 40 kya and more generally in the holocene, may have allowed anatomically modern humans to create highly elabo- rated cultures much along the line of Ayala’s (Chapter 16, this volume) hypothesis about morality. our hypothesis that culture was generally 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 difficult 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 sequencing genomes, is pro - viding important new tools. These methods promise two important contri- butions. First, they already help us to better understand paleodemography (rogers and harpending, 1992). second, 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 anatomically 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 genetic diversity. Coalescence times are older for autosomes than for mitochondria or y chromosomes in part because the effective pop- ulation size for diploid autosomes is four times the size of the population of maternally transmitted haploid mitochondria or paternally transmitted y chromosomes (Garrigan and hammer, 2006). 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 diver- sity farther away from our ancestral African homeland (vigilant et al., 1991; ramachandran et al., 2005; liu et al., 2006; handley et al., 2007; Wallace, Chapter 7, this volume). The populations most distant from one another, measured by the length of the most likely migration path from Africa, are most distant from one another genetically. Thus, the picture

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Gene–Culture Coevolution in the Age of Genomics /  of the genetic architecture of human populations derived from molecular methods bears a strong resemblance to that derived from classical human genetics (Cavalli-sforza et al., 1994). Africans maintain the most genetic diversity, and the most distant 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 efficient estimation methods for dating selective sweeps are those which use selectively neutral varia- tion to estimate population sizes and control for the effects of drift. The effects of selection on potentially nonneutral variation are then apparent as departures from expectations based on a neutral model (rogers, 2001; Williamson et al., 2005). To this point, limitations in the size and nature of the samples of sequenced human DnA do not allow high confidence 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. (2006) review the methods for detecting the action of selection on the genome on various timescales. on the longest timescales, selection is evidenced by functionally significant differences between species. For example, the FOXP2 gene has two functionally significant differences between humans and chimpanzees. Preliminary sequences of neandertal DnA suggest that we share these two changes with that spe- cies, 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, 250 kya, posi- tive selection leaves a signature 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 selec - tive sweep. At timescales 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 selection. As human populations left Africa and became exposed to divergent selection in different environments and cultures, different alleles would have been swept to high frequency in dif - ferent 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 sequence. The LCT regulatory gene down- regulates the secretion 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 lactase and to benefit from lactose. sequencing of the adult secretion variants of LCT from western

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0 / Peter J. Richerson et al. eurasia and Africa revealed that they were dysfunctional in different ways (Tishkoff et al., 2007b). Finally, at timescales less than 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 (2009) reviewed the promise and pitfalls of DnA sequence meth- ods based on 21 genome-wide scans for alleles under selection. To assess the reliability of these methods, Akey compared eight genome-wide scan studies using the hapMap and Perlegen databases. The eight studies reported a total of 5,110 distinct regions under selection, but only 14.1% were identified in two or more studies and 2.5% in four or more. never- theless, he finds grounds for cautious optimism. First, many of the genes that occur in multiple studies have already been firmly identified 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 tropical 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 adaptations to the new local environments into which humans were dispersing. significant issues remain. some reflect 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 dramatically (Grossman et al., 2010). A deeper difficulty 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 pigmentation 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. Functional 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 revolution- ized genomics also be applied to the expression of genes during develop-

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Gene–Culture Coevolution in the Age of Genomics /  ment, 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, exemplifying our still-primitive understanding of the connection between genotypes and phenotypes (Coop et al., 2008; Fisher and scharff, 2009). This gene, coding for a regulatory protein, has apparently been under strong selection since the last common ancestor with the other apes. Two amino acid substitu - tions have taken place in the hominin lineage. early reports from a study of language deficits 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 con- served gene that is expressed in a wide variety of tissues during vertebrate development. in the brain, a ChiP study shows that it down-regulates CNTNAP2, the gene encoding contactin-associated protein-like 2, a mem- ber of the neurexin superfamily. This gene is involved with cell recogni- tion 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 identified 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 substitutions in the derived human gene contains a high frequency of derived neutral variants that have not been disrupted by recombination, suggesting that the second of the two human substitutions on the gene must have taken place in the last 130 kya (Coop et al., 2008). on the other hand, Krause et al. (2007) sequenced neandertal 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) introgression between neandertals and anatomically modern humans (Plagnol and Wall, 2006), 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 (Coop et al., 2008; Ptak et al., 2009). Thus, although 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 intimidatingly 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 environmental variability has long been an important theme in gene–culture coevolu -

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 / Peter J. Richerson et al. 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 (2009) 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, emphasiz - ing 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 sup - ported by genetic specializations favoring different occupations. As cul - tures 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 differ- ing genotypes are better at different tasks (Mattila and seeley, 2007). 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 generating behav- ioral 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 something human brains evolved to do. rather, cultures evolved writing systems that take advantage of parts of the brain evolved to do quite different things (Dehaene, 2009). Cultures find ways to finesse 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 envi- ronment is falsified by the rapid secular increase in iQ in many developed countries during the 20th century (Flynn, 2007), and by the fact that iQ is much less heritable among populations with lower socioeconomic status (Turkheimer et al., 2003). likewise, iQ is correlated across countries with stage of modernization (newson and richerson, 2009). The amount and quality of education seem to explain most of the variation in iQ between groups and over time within groups (nisbett, 2009). Botticini and eckstein (2007) argue that a tradition of education and literacy accounts for Jews entering jobs requiring high intellectual skills. of course, this hypothesis and Cochran and harpending’s are not mutually exclusive. To what extent are the genes that underlie behavioral variation in humans evolving mostly

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Gene–Culture Coevolution in the Age of Genomics /  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 coevolution important? Theory points to the speed of cultural evolution compared with genetic evolution. even rudimentary culture capacities could sup- port appreciable amounts of culture-driven gene–culture coevolution. This idea is difficult 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 paleoanthropological 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 refu- tation of an early coevolutionary hypothesis proposed by sherwood Washburn (1959). Washburn speculated that a coevolutionary process was set up by the development of traditions of making simple stone tools. The use of tools created environments that favored the specialization of hands for toolmaking, leading toward upright posture. As hands became more specialized for toolmaking, selection would favor larger brains, including improved manual dexterity in fine 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. We illustrate how genomic data might help improve our understanding of hominin evolution in the Plio-Pleistocene. We first sketch the Plio-Pleistocene evolutionary events known from skeletons and artifacts and then conjecture about how genomic data might help resolve issues by the paleoanthropology of this period. Then we turn to the problems of the evolution of language and social organization.

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 / Peter J. Richerson et al. events in the evolution of these two especially important features of gene– culture coevolution have been difficult to reconstruct because the skeletal and artifact data regarding them are so enigmatic. here genomic data are likely to prove especially useful. The genome-wide scans for genes under selection in the last few tens of thousands of years described in the main text are based on single nucleotide polymorphisms (snPs) from a relatively limited sample of genomes. These data provide only a relatively low-resolution picture of genetic variation. The 1000 Genomes Project is in the process of fully sequencing at least 1,000 genomes from 11 populations representing the major regions of the world (http://www.1000genomes. org/page.php). The cost of such full sequences will probably continue to fall. over the next decade, a large representative sample of high-resolution sequences should be available. We can anticipate that the information in these sequences, together with advances in functional genomics, will offer great insights into the deep evolutionary history of our lineage. Selection in the Late Pleistocene To judge from paleoanthropological data, the period from ~250 kya to 50 kya was the time interval over which people became behaviorally modern. African populations had rather modern, but not completely mod- ern, skeletons and large brains early in this period (rightmire, 2009b), but mostly made comparatively simple stone tools until about 40 kya. About this time, anatomically modern Africans dispersed from Africa to eurasia. in western eurasia and northern Africa, anatomically modern populations began making sophisticated Upper Paleolithic stone tools and art objects about 40 kya. ephemeral episodes of more sophisticated tool making do occur much earlier in Africa (Jacobs et al., 2008). The early, if ephemeral, occurrence of sophisticated stone tools at the same time period as large- brained early modern humans is consistent with behavioral moderniza- tion being toward the beginning of this period. if so, the fact that anatomi- cally modern humans were confined for so long to Africa, usually making fairly simple stone tools, is puzzling. if people were capable of modern behavior, why did they so seldom exhibit it? Why was their dispersal out of Africa so late? Klein (2009) suggests that a fortuitous mutation perhaps ~60 kya led to the final modernization of humans and to our movement out of Africa. An uptick in the millennial- and submillenial-scale climate variation after about 70 kya might have advantaged the more cultural hominins and led to a substantial bout of gene–culture coevolution. or perhaps the explanation is entirely environmental and genes played little or no role. simply increasing human population densities in some times and places could support the evolution of more complex technology (henrich, 2004b; Powell et al., 2009).

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Gene–Culture Coevolution in the Age of Genomics /  As mentioned in the earlier, genomic studies have already revolution- ized our understanding of our migration out of Africa, following the pio - neering mitochondrial DnA phylogeny of Cann, stoneking, and Wilson (1987). By now it is clear that much of the genetic variation and genetic diversity in human populations is consistent with a spread out of Africa about 60–50 kya (ramachandran et al., 2005; liu et al., 2006). examples of genes that very likely came under selection in this period include genes affecting skin pigmentation (Mcevoy et al., 2006; Myles et al., 2007). As with genes selected in the holocene, different populations have reached parallel solutions to the same adaptive problem. The genes that underlie the light skin adaptation to increase vitamin D photosynthesis in cold, low-sunlight environments are different in eastern and western eurasia (Jablonski and Chaplin, Chapter 9, this volume). ideally, genomic data will provide an accurate timescale for major evolutionary events, which can then be used in conjunction with paleo - anthropological data to resolve some of the puzzles noted above. This quest for well-dated selection events will require more data and improved methods. The best tool for younger events, dates estimated from the long haplotypes associated with genes under selection, is nearly erased by recombination in this earlier period. The reduced diversity and excess of rare haplotypes in the regions flanking genes under selection in theory will lead to datable genomic events in this time period (sabeti et al., 2006). An interesting example of another kind of data that might prove useful is the study of the evolution of human commensals and parasites. For example, the human body louse lives in clothing but feeds on the body. it evolved from the head louse, which lives in hair, 72 kya ± 42 kya (Kittler et al., 2003). Thus, clothing must have evolved fairly recently, perhaps associ - ated with the out-of-Africa migration of anatomically modern humans to higher latitudes. Aside from the human genome itself, we wonder how much evolutionary history might be reconstructed from the diverse micro- flora that inhabit our digestive tract and skin (hattori and Taylor, 2009). Complete sequences of neandertal autosomal DnA promise to revo- lutionize our understanding of selection in the late Pleistocene (Green et al., 2006). improvements in the database of fossil mitochondrial DnA sequences also promise much (Krause et al., 2010). Assuming that the ancestral Homo heidelbergensis population that gave rise to neandertals and ourselves lived around 200–600 kya (Weaver et al., 2008), and if there was no introgression of genes from neandertals to anatomically modern humans (or that such introgression as did occur is detectable), then any genetic variants that we share with neandertals (such as, possibly, the derived FOXP2 variant) must have had its origin before the date of sepa- ration of the two species. Derived genes not shared with neandertals are candidates to have evolved on the anatomically modern lineage. We might

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0 / Peter J. Richerson et al. not want to discount the possibility of convergent evolution in the two species. neandertals had brains as large as anatomically modern humans (Klein, 2009). By some accounts, neandertals proved as capable of sophis- ticated culture as anatomical moderns. Just before we came into contact with them, and after the uptick in millennial- and submillennial-scale variation ~60 kya, neandertals may have independently evolved the mod- ern behaviors ascribed to the makers of the Upper Paleolithic industries of western eurasian anatomical moderns (d’errico, 2003; Zilhão et al., 2010). introgression between anatomically modern humans and neandertals is a possibility (Cochran and harpending, 2009), and what genes did intro- gress would be informative if they can be reliably detected, particularly if they generated parallel selective sweeps in the two species. For this period, we have nothing like the unmistakable signature of cultural changes driving genetic changes that we see in the holocene. if anything, genetically determined traits such as brain size seem to appear in the paleoanthropological record preceding, rather than following, the most conspicuous cultural changes. Perhaps the most interesting single question here is whether genes underlying modern behavior evolved early or late in this period. The durable artifacts tend to support a late interpreta - tion, because a great number of traits that are most diagnostic of modern behavior, such as symbolic behaviors (art), develop rather late. if nean- dertals did independently evolve modern behavior, then perhaps parallel or convergent genetic or cultural responses to increased climate variation can explain the pattern. The capacity for modern behavior need not nec - essarily have been present in the last common ancestor. The skeletons of early anatomically modern humans are still very robust and nonmod- ern in other ways (rightmire, 2009b). The fossils and stone tools do not necessarily contradict the hypothesis that large-brained but archaic ana - tomical modern genes were coevolving in response to Middle Paleolithic cultural innovations. The combination of large brains and comparatively simple technology is a major puzzle nonetheless. how were our ancestors supporting such an energetically expensive organ unless by modern or near-modern behavior? even the anatomically modern humans that left Africa and moved eastward to eastern eurasia and Australia did so using relatively simple Middle Paleolithic toolkits (Foley and lahr, 1997). The most dramatically modern Upper Paleolithic industries rich in symbolic artifacts were seemingly confined to western eurasia and northern Africa for tens of thousands of years after 40 kya. The especially intense pattern of millennial- and submillennial-scale variation after 70 kya suggests that environmental conditions potentially played some role. We might imagine that the adaptive advantages of Middle Paleolithic stone tool traditions were sufficient to induce the evo - lution of very large brains in both anatomical moderns and neandertals.

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Gene–Culture Coevolution in the Age of Genomics /  Perhaps the achievement of ephemeral sophisticated industries in Africa before 70 kya, and later more permanently in western eurasia, depended upon larger populations, leading to the ability to accumulate more innova- tions. rather than a bottleneck around 70 kya as mitochondrial coalescence data suggest, perhaps human populations were chronically rare before 70,000 kya. imagine that humans were competing in a rather crowded guild of top carnivore species: lions, leopards, cheetahs, and other large cats; hyenas; wild dogs; wolves; and bears. More variable environments, to which humans could adapt culturally, might have given our species a competitive advantage. An increase in millennial- and submillennial-scale climate variation might thus have led to the spread of moderns out of Africa, and to population densities high enough to lead to Upper Paleo - lithic and similar industries (richerson et al., 2009). Selection from the Late Pliocene to Middle Pleistocene events deeper in the evolution of hominins are naturally even more opaque. The interesting high-frequency part of the paleoclimate record is seriously deficient for this period. During the long period from about 2.6 to 1 million years ago, when the low-resolution record was dominated by the 41,000-year cycle, early members of our own genus Homo enter the fossil record, particularly H. erectus sensu lato. These populations had relatively modern postcrania and brain sizes relative to body sizes inter- mediate between Australopithecines (and living apes) and anatomically modern humans and neandertals (ruff et al., 1997). Many, if not most, of the major genetic changes between humans and the rest of the apes probably occurred in this period, during the transitions from Australo- pithecines to H. habilis and from H. habilis to H. erectus. According to some interpretations, H. erectus had a rather modern physique and an enlarged brain relative to body size (Mchenry and Coffing, 2000). subsistence activities might have included a considerable ability to acquire meat and fat from hunting. For example, an important component of human hunt- ing is the ability to run down large- and medium-sized game. humans from H. erectus onward could probably run efficiently and sweat to keep our body temperature down during extended exercise. H. erectus hunters could thus probably have run medium-sized herbivore prey until they were exhausted or overheated or both, and then dispatched them with unsophisticated weapons (Bramble and lieberman, 2004; liebenberg, 2006; Jablonski and Chaplin, Chapter 9, this volume). We can expect to find genes related to a large variety of specifically human traits to have evolved in this period, but in most cases we will have to entertain the hypotheses that they evolved earlier in Australopithecines or in post- H. erectus hominins.

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 / Peter J. Richerson et al. early Homo skeletal material is loosely associated with two successive tool traditions, the oldowan and the Acheulean. H. erectus spread out of Africa and into island southeast Asia, tolerating temperate climates and apparently crossing deep water, apparently some 1.7 mya (rightmire et al., 2006). some authorities emphasize the expedient simplicity of the old- owan and early Acheulean industries. De la Torre and colleagues (2003, 2008) argue that a rather sophisticated appreciation of the properties of stone, and a fairly sophisticated approach to knapping, characterized these two industries. sharon (2009) presents evidence that Acheulean makers of large biface tools had efficient and culturally variable techniques for pro - ducing these signature artifacts. A recently published Acheulean campsite dating to 750 kya seems to have been fairly complex. it contained remains suggesting that H. erectus could exploit a wide variety of plant and animal resources, including fish and acorns, and that they controlled fire (Alper- son-Afil et al., 2009). evidence for still-earlier use of fire is controversial (Wrangham, 2009). interestingly, reports on living individuals with pri- mary microcephaly (small brains but without organizational disruptions) indicate that they suffer only mild to moderate mental retardation (Cox et al., 2006). Perhaps these brains are a clue to the cognitive capabilities of H. erectus. H. erectus’s brain architecture and behavior might have been rather modern in many respects. Donald (1991) suggests that H. erectus had advanced abilities to imitate motor patterns but still lacked speech. he reviews 19th-century data on deaf mutes as evidence that alinguistic people would be capable of imitating many if not most modern skills except ones directly dependent on language. Thus, culture-led gene–cul - ture coevolution could have been an active process in this period. After 1 mya, the 100-ky cycle came to dominate the low-frequency component of the climate record. early in this period, larger-brained hominins, often lumped into the taxon H. heidelbergensis, evolved in Africa and western eurasia (rightmire, 2009a). Thus, there are hints, but at this point only bare hints, that changes in climate variation were increasing selection in favor of more sophisticated culture capacities. some progress has been made on the representation of tool use in the brain (Peeters et al., 2009). Many genes associated with the ability to make and use tools probably evolved during this long period. since the sequencing of the chimpanzee genome, a considerable amount of effort has gone into searching for the differences between the two species (Kehrer-sawatzki and Cooper, 2007; Portin, 2007, 2008; varki and nelson, 2007). Many candidates for genes that have come under selection have turned up in these comparisons. some of the appar- ently most interesting genes, such as copy number in the gene MGC8902, have unknown function. The large or family of genes (~1,000–1,400 loci) involved in odor perception has a very high percentage of nonfunctional

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Gene–Culture Coevolution in the Age of Genomics /  genes in humans, although some specific genes seem to have undergone positive selection. This pattern of loss of function of olfactory genes is related to the reduced area of olfactory epithelium and relatively small olfactory bulb in humans. likely enough, the development of cooking and the use of cultural traditions to identify suitable food items reduced our dependence on olfaction. The beginning of cooking likely also caused major changes in human diets which should be reflected in the genome (Wrangham, 2009). our Australopithecine ancestors were probably largely herbivo- rous. early species of Homo were probably generalist omnivores with significant access to hunted and scavenged fat and meat (Ungar et al., 2006). By Middle and Upper Paleolithic times, stable isotope analysis and zooarchaeological remains suggest that humans were highly carnivorous (stiner, 1992; richards et al., 2001). The expansion of brains in Homo was very likely tied to improved nutrition via hunting and cooking (leon- ard et al., 2007). Genes associated with dietary changes and brain-size increase should be correlated to each other and to patterns derived from paleoanthropology. Evolution of Language and Social Organization language and social organization were probably closely related in the course of human evolution. Much of our use of language is related to social life, and it is reasonable to assume considerable parallelism in their evolu - tion (Dunbar, 1996). They are both features that fossilize poorly. inferences about their presence or absence are not easy to make. For example, Philip lieberman (2007) has long argued from anatomical evidence regarding the shape of the vocal tract that the capacity to clearly articulate modern vowel systems only emerged around 50 kya. he nevertheless thinks that ancient species of Homo had some useful capacity for speech. indeed, there is perhaps a consensus among evolutionists writing on language that it evolved by culture-led gene–culture coevolution over an extended portion of our evolutionary history (richerson and Boyd, in press). nev- ertheless, dissenters on this point certainly exist. For example, Tattersall (2007) argues that articulate language must have originated only 50 kya. he cites not only the anatomical evidence but also the late first finds of unambiguous symbolic artifacts such as art. Those who imagine that language arose by prolonged culture-led coevolution differ greatly in the details of their scenarios. For example, Pinker (2003) argues that coevolu - tion will lead to complex innate cognitive specializations for language. Kirby et al. (2007) use simulations to illustrate how the basic features of language might be cultural adaptations to preexisting cognitive con- straints on language learning. That is, language evolved to fit our brain,

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 / Peter J. Richerson et al. rather than the other way around (Deacon, 1997). if cultural adaptation is sufficiently powerful, it might lead to little or no coevolutionary pressure on innate cognitive mechanisms. Tomasello (2008) argues that language is a cultural construct and that most of the coevolved innate predisposi- tions for language are shared with other cultural features. Although the involvement of the FOXP2 gene in language evolution has turned out to be complex and controversial, the intense interest it has generated illus - trates the questions we hope to answer with the help of genomic methods: What genes changed, when did they change, and what is the functional significance of the changes? Many scenarios have been advanced in discussions of the evolution of social organization, although it has not received the same amount of atten- tion as language. lovejoy (2009) argues that reduced canines in the pos- sible ancestral hominin Ardipithecus ramidus indicate that this early species already exhibited reduced intrasexual antagonism and greater social adhe- sion on the part of both males and females. hrdy (2009) reviews a large body of evidence regarding the role of cooperative breeding (assistance to females with dependent offspring by others), concluding that cooperative breeding must have evolved in the hominin lineage before brain enlarge - ment. The costly big brains and long juvenile periods of great apes already strain the ability of mothers to rear such offspring. Despite having highly dependent infants needing to grow even larger brains, human interbirth intervals are shorter than those of great apes, something only possible with alloparental assistance. Burkart et al. (2009) argue that cooperative breeding would have laid the initial basis for cooperative psychological predispositions in humans. interesting progress has been made on the pos- sible role of a vasopressin receptor gene polymorphism in human bonding (Walum et al., 2008). The comparative biology of human reproduction sug- gests that humans experience relatively low sperm competition, an indica - tion of male investment in provisioning offspring rather than competing for mates (Anderson et al., 2005; Martin, 2007). Derived alleles for genes expressed in testes and sperm turn up in scans for evidence of selective differences between humans and chimpanzees (nielsen et al., 2005). however, much genetic change also appears to have happened in the late Pleistocene and even in the holocene according to data we have reviewed in this chapter. Perhaps important innovations involving social predispositions occurred as late as 50 kya (Klein, 2009) or even in the holo- cene (Cochran and harpending, 2009). once again, the evidence for just how far back in time the culture-led mode of gene–culture coevolution can be pushed is an open question to which evolutionary genomics will have much to contribute. As with language, not only is timing of important events uncertain but also the division of labor between genes and culture. We (richerson and Boyd, 1998, 1999) have suggested that humans’ social

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Gene–Culture Coevolution in the Age of Genomics /  psychology was fairly extensively remodeled by gene–culture coevolu- tion. however, in ethnographically known societies, culturally transmit - ted norms and institutions do much heavy lifting. We do not anticipate finding that dramatic genetic changes were necessary to accompany the evolution of social complexity in the holocene. The simpler societies known ethnographically rely heavily on norms and institutions to regulate social life, so no revolution in our innate psychology seems necessary to account for complex societies. Cosmides et al. (Chapter 15, this volume) suggest that much more of the load is carried by content-rich cognitive adaptations than by transmitted culture. Functional and developmental genomics should eventually lay a foundation for understanding the roles of genes and culture in current behavior and in the past evolution of cur- rent behavioral capacities. CONCLUSIONS Genomics has already made quite substantial contributions to our understanding of human evolution, beginning with the use of mitochon - drial DnA variation to understand the timing of events in recent human evolution and to provide a window into human paleodemography, includ- ing past population sizes and migration patterns. The use of linkage disequilibrium to identify genes under recent selection suggests a mas - sive holocene wave of genetic change initiated by the cultural evolu- tion of agricultural subsistence. even here, our lack of knowledge of the functional significance 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 under- standing. 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 contribu - tion 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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