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Nonadaptive Processes in Primate and Human Evolution

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Nonadaptive Processes in Primate and Human Evolution YEARBOOK OF PHYSICAL ANTHROPOLOGY 53:13–45 (2010) Nonadaptive Processes in Primate and Human Evolution Eugene E. Harris* Department of Biological Sciences and Geology, Queensborough Community College, City University of New York, Bayside, NY 10364 KEY WORDS genetic drift; positive selection; purifying selection; effective population size; neutral theory; selective constraint; gene duplication; compensatory substitution ABSTRACT Evolutionary biology has tended to focus potential consequences of these effects for primate and on adaptive evolution by positive selection as the pri- human evolution. For example, an increase in the fixa- mum mobile of evolutionary trajectories in species while tion of slightly deleterious mutations could potentially underestimating the importance of nonadaptive evolu- have led to an increase in the fixation rate of compensa- tionary processes. In this review, I describe evidence tory mutations that act to suppress the effects of slightly that suggests that primate and human evolution has deleterious substitutions. The potential consequences of been strongly influenced by nonadaptive processes, par- compensatory evolution for the evolution of novel gene ticularly random genetic drift and mutation. This is evi- functions and in potentially confounding the detection of denced by three fundamental effects: a relative relaxa- positively selected genes are explored. The consequences tion of selective constraints (i.e., purifying selection), a of the passive accumulation of large-scale genomic muta- relative increase in the fixation of slightly deleterious tions by genetic drift are unclear, though evidence sug- mutations, and a general reduction in the efficacy of pos- gests that new gene copies as well as insertions of trans- itive selection. These effects are observed in protein-cod- posable elements into genes can potentially lead to ing, regulatory regions, and in gene expression data, as adaptive phenotypes. Finally, because a decrease in well as in an augmentation of fixation of large-scale selective constraint at the genetic level is expected to mutations, including duplicated genes, mobile genetic have effects at the morphological level, I review studies elements, and nuclear mitochondrial DNA. The evidence that compare rates of morphological change in various suggests a general population-level explanation such as mammalian and island populations where Ne is reduced. a reduction in effective population size (Ne). This would Furthermore, I discuss evidence that suggests that cra- have tipped the balance between the evolutionary forces niofacial morphology in the Homo lineage has shifted of natural selection and random genetic drift toward from an evolutionary rate constrained by purifying selec- genetic drift for variants having small selective effects. tion toward a neutral evolutionary rate. Yrbk Phys After describing these proximate effects, I describe the Anthropol 53:13–45, 2010. VC 2010 Wiley-Liss, Inc. Although we are nearly 99% similar to chimpanzees in Americas; see Cavalli-Sforza et al., 1994). Much less nucleotide sequence, phenotypically we appear to have explored has been the role of random genetic drift in diverged considerably farther from our common ancestor. influencing the evolution of primates, and humans in Our unique human traits include bipedal walking, particular. increased manual dexterity, increased brain size, The well-known neutralist versus selectionist contro- reduced body hair, and our ability to make and use tools versy in evolutionary genetics is essentially a debate and complex language. Most efforts to understand the about whether evolutionary change is mostly due to evolution of these features have emphasized adaptive genetic drift acting on neutral variation, or whether it is evolution as the most important, if not singular, evolu- due to selection acting on adaptive variation (Ford, 1964; tionary force. Yet, adaptive evolution is only one of the Kimura, 1968, 1969; King and Jukes, 1969; Lewontin, forces of evolutionary change, others being mutation, 1974; Gillespie, 1991; Kreightman, 1996; see Nei, 2005). random genetic drift, and recombination. These forces The controversy has subsided somewhat since its most are described as nonadaptive because the evolutionary vociferous days in the 1970s and 80s but has not reached change they produce is due to factors unrelated to indi- resolution (see Hey, 1999; Crow, 2008; Hahn, 2008). In- vidual differences in relative fitness. The importance of terest in this issue, however, has reignited within the nonadaptive forces in influencing evolutionary change is last decade in the context of analyses of large amounts becoming increasingly clear (Stoltzfus, 1999, 2006; Koo- of genome-wide DNA data from humans and other nin, 2004, 2009a,b; Hughes, 2007, 2008, 2009; Lynch, 2007a,b; Stoltzfus and Yampolsky, 2009; Ellegren, 2009). *Correspondence to: Eugene E. Harris, Department of Biological Within anthropological and human genetics, random Sciences and Geology, Queensborough Community College, City genetic drift has most often been studied with respect to University of New York, 222-05 56th Avenue Bayside, NY 11364. founder effects on isolate populations (e.g., Hutterites, E-mail: [email protected] Old Order Amish, Ashkenazi Jews, Yanomamo etc.; see Smouse et al., 1981; Sokal et al., 1986; Arcos-Burgos and DOI 10.1002/ajpa.21439 Muenke, 2002; Risch et al., 2003; Slatkin, 2004) as well Published online in Wiley Online Library as in bottleneck events (e.g., first migration into the (wileyonlinelibrary.com). VC 2010 WILEY-LISS, INC. 14 E.E. HARRIS species. Through analyses of these data, it is becoming larger Ne, with estimates ranging from 104K to 157K increasingly revealed that the population size of a spe- (Chen and Li, 2001; Burgess and Yang, 2008). Estimates cies, specifically its long-term effective population size of Ne in the human H/C/gorilla (G) ancestral population (Ne), is fundamental in determining the relative impor- range from 55K to 83K, and estimates for the ancestral tance of genetic drift and selection. Furthermore, it is H/C/G/orangutan population range from 84K to 126K becoming clear that the relative power of these forces (Burgess and Yang, 2008). These estimates indicate an has varied in different animal lineages (for discussion approximately 10-fold reduction in Ne in the course of see Ellegren, 2009). The findings are presumably human evolution, a reduction that seems to be extreme explained by population genetics theory that posits a for a primate species. central role of Ne in influencing the relative importance Although few good estimates of Ne exist for nohuman of these two evolutionary processes. Explained briefly, primates, it is generally assumed that Ne is reduced gen- when molecular variants have large selective coeffi- erally in primates compared with other animal groups. cients, either because they are strongly advantageous or Recent analyses of polymorphism in macaques estimate strongly deleterious, natural selection can act as a that Ne is approximately 70,000 (Hernandez et al., powerful force in shaping the direction of molecular 2007). In contrast, estimates of Ne in murids (mice and evolution. However, if most variants have only slight rats) are placed at around 450K–820K (Eyre-Walker et al., effects on fitness, a finding that has become increasingly 2002). Although more distantly related, Drosophila species, supported (Ohta, 1973, 1974, 2003; Hughes et al., 2003, which have effective population sizes an order of magnitude 2005; Eyre-Walker et al., 2006a; Eyre-walker and larger than mammal species (1–2 million; see Eyre-Walker Keightley, 2007), then the extent to which natural selec- et al., 2002), they provide a useful contrast for studying the tion can discriminate these variants is a function of Ne. evolutionary effects of differences in population size. For these variants, Ne becomes the critical determining A reduction in Ne in the evolution of primates and factor that tips the balance between either natural selec- more so in the course of human evolution is expected to tion being the dominant evolutionary force acting on have had considerable effects on the dynamics of molecu- them, or random genetic drift becoming the dominant lar evolution. The reduction is expected to have aug- force. When Ne is sufficiently small, the effects of genetic mented the relative power of random genetic drift rela- drift dominate over natural selection and completely tive to natural selection. This, in turn, is expected to have determine the fate of these variants. This theory is its greatest effects on slightly deleterious variants, both known as the Nearly Neutral Theory by Tomoko Ohta increasing the fixation of these variants by genetic drift (1973, 1974), which is an extension of Motoo Kimura’s during divergence, and in permitting slightly deleterious Neutral Theory Of Molecular Evolution (Kimura, 1968, variants to increase in frequency in recent human popula- 1969, 1983). On the other hand, if Ne is sufficiently tions. These predictions are supported by studies making large, natural selection is better able to discriminate the large-scale genomic comparisons between primates and selective effects of genetic variants, tending to promote other species (Eyre-Walker et al., 2002; Keightley et al., advantageous variants while removing deleterious var- 2005a,b; Kryukov et al., 2005) and in genome-wide analy- iants, even if these have only slightly negative selective ses of polymorphism within human populations (Fay
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