Neutral Theory and the Evolution of Human Physical Form: an Introduction to Models and Applications
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doi 10.4436/jass. 96009 JASs Invited Reviews e-pub ahead of print Journal of Anthropological Sciences Vol.Vol. 9696 (2018),(2018), pp.pp. 1-207-26 Neutral theory and the evolution of human physical form: an introduction to models and applications Timothy D. Weaver Department of Anthropology, University of California, Davis, CA 95616, USA e-mail: [email protected] Summary -– Anthropologists have long been interested in explaining patterns of variation in human physical form, in both present-day and ancient humans. Starting in the 1950s, their explanations became more firmly rooted in evolutionary theory, but they have typically focused on adaptive accounts. Neutral explanations – those grounded in models of evolution by mutation, genetic drift, and gene flow rather than natural selection – provide an alternative to adaptive explanations, and in recent years, neutral models have become an important tool for researchers investigating the evolution of human physical form. Neutral models have implications for many areas of biological anthropology, including using morphology to reconstruct the histories and migrations of recent human populations, using morphology to infer the evolutionary relationships among hominin taxa, and clarifying how natural selection has acted on physical form throughout human evolution. Their application to anthropological questions has stimulated biological anthropologists to more seriously consider the roles of history and chance in human evolution. In light of the growing importance of neutral explanations in biological anthropology, the goal here is to provide an introduction to neutral models of phenotypic evolution and their application to human physical form. Keywords –- Human evolution, Human variation, Genetic drift, Mutation, Gene flow, Coalescence. Introduction form became more firmly rooted in evolutionary theory, but they have typically focused on adap- Anthropologists have long been interested tive explanations (e.g., Washburn, 1951). in explaining patterns of variation in human Neutral models – models of evolution by physical form, in both present-day and ancient mutation, genetic drift, and gene flow rather humans. Indeed, one major division of anthro- than natural selection – for protein and subse- pology, physical anthropology, initially con- quently DNA-sequence evolution were first pro- cerned itself almost exclusively with human posed in the 1960s and 1970s (Kimura, 1968; physical form, skeletal morphology in particu- King & Jukes, 1969; Kimura & Ohta, 1971), lar (Boas, 1899; Hrdlicka, 1908), before this and these foundational neutral models were fol- field diversified into other areas, such as genet- lowed by neutral models of phenotypic evolution ics, non-human primate behaviour and ecology, in the 1970s and 1980s (Lande, 1976; Lynch & and human biology, and began to be commonly Hill, 1986; Turelli et al., 1988). Although the called biological anthropology. As von Cramon- earliest neutral models considered only mutation Taubadel (2014) recently reviewed in this journal and genetic drift, subsequent ones also included in her article about human cranial morphology, gene flow (e.g., Kimura & Maruyama, 1971; early views of human physical form were typo- Lynch, 1988a). Neutral models forever changed logical, with the goals of identifying the charac- evolutionary biology, perhaps most significantly teristics of different human groups and classify- because they highlighted that evolution and ing individuals (e.g., Hooton, 1926). Starting natural selection are not synonyms, which forced in the 1950s, investigations of human physical researchers to evaluate adaptive explanations the JASs is published by the Istituto Italiano di Antropologia www.isita-org.com 28 Neutral theory and human physical form Tab. 1 - Definition of mathematical terms. against an alternative to natural selection that was often difficult to dismiss. Additionally, it became clear that even if one was primarily interested tg split time in generations in adaptive changes, neutral models provided a g generation length foundation for any evolutionary investigation, ¯ xi mean of a single phenotypic trait in group i because natural selection will act in concert with x¯ grand mean (mean of the group means) of a the neutral evolutionary processes of mutation, single phenotypic trait genetic drift, and gene flow. d number of groups Neutral models began to make inroads into i number of steps separating two groups in a studies of human physical form in the 1980s and circular stepping-stone model 1990s (Rogers & Harpending, 1983; Lynch, ds number of sampled groups 1989; Relethford, 1994), and they became a VW within-group phenotypic variance prevalent tool in these investigations in the VB between-group phenotypic variance 2000s (reviewed by Roseman & Weaver, 2007; h2 (narrow sense) heritability von Cramon-Taubadel & Weaver, 2009). Many V 2 WA within-group additive genetic variance (h VW) of these studies of human physical form were N population size (number of breeding individuals) based on the global dataset of human cranial var- of each group iation collected by Howells (1973, 1989, 1995). Ne effective population size of each group Neutral models provide a theoretical basis for 2 σm additive genetic variance introduced by mutation using morphology to reconstruct the history and B between-group phenotypic variance-covariance structure of recent human populations and the matrix evolutionary relationships among hominin taxa. P within-group phenotypic variance-covariance They can be used as a baseline against which to matrix evaluate adaptive hypotheses about human phys- G within-group additive-genetic covariance-matrix ical form. Perhaps most fundamentally, studies U additive genetic variances and covariances demonstrating the importance of neutral mod- introduced by mutation els to anthropological questions have stimulated τW average coalescence time of pairs of alleles from biological anthropologists to more seriously con- the same group sider the roles of history and chance in human τB average coalescence time of pairs of alleles from different groups evolution. τ average coalescence time of pairs of alleles With this background in mind, the goal here from the collection of groups sampled is to provide an introduction to neutral models M/2 proportion of individuals exchanged each of phenotypic evolution and their application generation by two adjacent groups, in each to human physical form. More detailed descrip- direction tions of specific neutral models can be found else- FST measure of genetic differentiation calculated where, but there is currently no single source that from genetic data gathers together the models relevant to biologi- QST measure of genetic differentiation calculated cal anthropological investigations and discusses from experimental phenotypic data the connections among them. The mathematical PST measure of genetic differentiation calculated from observational phenotypic data terms used in the paper are defined in Table 1 and c scale factor for the between-group phenotypic as they are discussed. Table 2 provides a glossary variance of terms from quantitative and population genet- ΔA difference between two groups in their additive- ics and evolutionary biology (see also Relethford, genetic-effect means 2007; Konigsberg, 2012; von Cramon-Taubadel, ΔO difference between two groups in their other- 2014). Table 3 gives brief explanations for how effect (dominance genetic, key quantitative and population genetic param- interaction genetic, environmental) means eters can be estimated. 2 Neutral theory and human physical form T. D. Weaver 39 Tab. 1 - Definition of mathematical terms. against an alternative to natural selection that was Tab. 2 - Glossary. often difficult to dismiss. Additionally, it became clear that even if one was primarily interested Adaptive evolution. Typically, adaptive evolution refers to evolution (change) due to natural selection, and this is tg split time in generations in adaptive changes, neutral models provided a how this phrase is used here. However, adaptive – and therefore adaptive evolution – is not defined the same way by g generation length foundation for any evolutionary investigation, all evolutionary biologists. See also neutral evolution. ¯ xi mean of a single phenotypic trait in group i because natural selection will act in concert with Additive genetic variance. Variation among individuals for a particular trait is typically quantified by variance, which is the average squared deviation of each individual from the mean (average). Additive genetic variance is the fraction x¯ grand mean (mean of the group means) of a the neutral evolutionary processes of mutation, of the variance that is due to additive genetic effects, which excludes genetic variance from genetic interactions be- single phenotypic trait genetic drift, and gene flow. tween alleles at the same locus (dominance effects) or different loci (epistatic effects). Evolutionary quantitative genetic d number of groups Neutral models began to make inroads into models focus on additive genetic variance because recombination tends to break down genetic interactions across gen- erations. Variance also results from environmental effects. See also environmental variance and phenotypic variance. i number of steps separating two groups in a studies of human physical form in the 1980s and circular stepping-stone model Allele. The genome of any particular individual can be divided up into different locations, or loci, on the individual’s chro-