Academic journal article Genetics

Sex-Linked Inheritance in Macaque Monkeys: Implications for Effective Population Size and Dispersal to Sulawesi

Academic journal article Genetics

Sex-Linked Inheritance in Macaque Monkeys: Implications for Effective Population Size and Dispersal to Sulawesi

Article excerpt

ABSTRACT

Sex-specific differences in dispersal, survival, reproductive success, and natural selection differentially affect the effective population size (N^sub e^) of genomic regions with different modes of inheritance such as sex chromosomes and mitochondrial DNA. In papionin monkeys (macaques, baboons, geladas, mandrills, drills, and mangabeys), for example, these factors are expected to reduce N^sub e^ of paternally inherited portions of the genome compared to maternally inherited portions. To explore this further, we quantified relative N^sub e^ of autosomal DNA, X and Y chromosomes, and mitochondrial DNA using molecular polymorphism and divergence information from pigtail macaque monkeys (Macaca nemestrina). Consistent with demographic expectations, we found that N^sub e^ of the Y is lower than expected from a Wright-Fisher idealized population with an equal proportion of males and females, whereas N^sub e^ of mitochondrial DNA is higher. However, N^sub e^ of 11 loci on the X chromosome was lower than expected, a finding that could be explained by pervasive hitchhiking effects on this chromosome. We evaluated the fit of these data to various models involving natural selection or sex-biased demography. Significant support was recovered for natural selection acting on the Y chromosome. A demographic model with a skewed sex ratio was more likely than one with sex-biased migration and explained the data about as well as an ideal model without sex-biased demography. We then incorporated these results into an evaluation of macaque divergence and migration on Borneo and Sulawesi islands. One X-linked locus was not monophyletic on Sulawesi, but multilocus data analyzed in a coalescent framework failed to reject a model without migration between these islands after both were colonized.

THE effective size of a population (Ne) determines the relative impact of genetic drift and natural selection on mutations with mild effects on fitness (Charlesworth 2009). Differences in Ne are hypothesized to affect virtually every aspect of genome evolution, including rates of molecular evolution, abundance of introns and transposable elements, and persistence of duplicate genes, and this has important implications for the evolution of complexity via both adaptive and degenerative processes (Lynch 2007). Of relevance are not only the number of different individuals in a population, but also the number of copies of a gene within each individual. In diploid species with separate sexes, sex chromosomes and mitochondrial DNA (mtDNA) differ in copy number from autosomal DNA (aDNA): both sexes have two alleles at autosomal loci whereas in species with male heterogamy, males have one X and one Y chromosome, females have two Xs, and a female/male pair has effectively only one copy of mtDNA due to maternal inheritance. Sexspecific differences in demographic parameters such as migration, adult sex ratio, and variance in reproductive success also affect relative copy number and associated levels of neutral polymorphism at mtDNA, aDNA, the X chromosome (xDNA), and the Y chromosome (yDNA) (Hedrick 2007).

The effective population size is the number of individuals in aWright-Fisher idealized population (Fisher 1930; Wright 1931) that have the same magnitude of genetic drift as an observed population, where ideal individuals are diploid, and have discrete (nonoverlapping) generations, constant population size, and random mating. Ne can be quantified in terms of variance in allele frequency over generations (variance Ne) or variance in inbreeding over time (inbreeding Ne). If population size is constant with random mating, these approaches for quantifying Ne produce identical results (Kimura and Crow 1963; Whitlock and Barton 1997). At mutation-drift equilibrium with an equal number of males and females and a Poisson distributed number of offspring with a mean of two offspring per individual, Ne-aDNA and Ne-xDNA are expected to be four and three times as large, respectively, as Ne-yDNA and Ne-mtDNA; we refer to this as the "ideal expectation with an equal proportion of males and females. …

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