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

Abstract

Sex-specific differences in dispersal, survival, reproductive success, and natural selection differentially affect the effective population size (N 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 e of paternally inherited portions of the genome compared to maternally inherited portions. To explore this further, we quantified relative N 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 e of the Y is lower than expected from a Wright-Fisher idealized population with an equal proportion of males and females, whereas N e of mitochondrial DNA is higher. However, N 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.T HE effective size of a population (N e ) determines the relative impact of genetic drift and natural selection on mutations with mild effects on fitness (Charlesworth 2009). Differences in N e 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...

Evolutionary history of mountain voles of the subgenus Aschizomys (Cricetidae, Rodentia), inferred from mitochondrial and nuclear markers

“…One process with the potential to cause discordance between gene trees and species trees is lineage sorting; lineage sorting occurs as a result of the coalescent process, and is likely to result in discordance when population sizes are large or when times between splitting events are short (Maddison 1997). Other factors that can lead to discordance include: (i) introgressive hybridization resulting from gene flow between differentiated lineages (Klymus et al 2010); (ii) differential selective sweeps in mitochondrial versus nuclear DNA markers (Evans et al 2010); and/ or (iii) the effects of sex-biased dispersal on patterns of genetic structure in maternally vs biparentally inherited markers (Lampert et al 2003). We used coalescent simulations in JML (Joly 2012) to test whether discordance across loci could be explained by lineage sorting alone, or whether other processes must be involved.…”

The Biogeography of Sulawesi Revisited: Is There Evidence for a Vicariant Origin of Taxa on Wallace's “Anomalous Island”?

“…However, here as well as in some other cases (Ruedi et al 1998), the geographic coverage of sampling on Sulawesi is poor. In taxa such as the macaques or the wild boar, the different Sulawesi lineages do not occur sympatrically, but it is doubtful whether monophyly of the Sulawesi taxa can be ruled out, either because there is insufficient support of the respective nodes (wild boars, Larson et al 2005) or because nuclear data are in conflict with the mtDNA gene trees on this point (macaques, Tosi et al 2003;Evans et al 2010). Not only is there no obvious respective pattern in the distribution of lineages that have colonized Sulawesi independently, there is in our opinion also little hard evidence for any Sulawesi clade being confined to part of the island only, which might suggest a link of its origin on Sulawesi and tectonic processes.…”

The Condition Dependency of Fitness in Males and Females: The Fitness Consequences of Juvenile Diet Assessed in Environments Differing in Key Adult Resources

“…Even if the variation in condition is entirely environmental, stronger selection on condition in males will tend to exaggerate the intersexual difference in the variance of reproductive success. This causes additional differences between autosomal and sex-linked genes in the amount of drift they experience, affecting patterns of neutral diversity and adaptation (Storz et al 2001;Laporte and Charlesworth 2002;Hedrick 2007;Vicoso and Charlesworth 2009;Evans et al 2010).…”