Finding the Factors of Reduced Genetic Diversity on X Chromosomes of Macaca Fascicularis: Male-Driven Evolution, Demography, and Natural Selection

By Osada, Naoki; Nakagome, Shigeki et al. | Genetics, November 2013 | Go to article overview

Finding the Factors of Reduced Genetic Diversity on X Chromosomes of Macaca Fascicularis: Male-Driven Evolution, Demography, and Natural Selection


Osada, Naoki, Nakagome, Shigeki, Mano, Shuhei, Kameoka, Yosuke, Takahashi, Ichiro, Terao, Keiji, Genetics


ABSTRACT The ratio of genetic diversity on X chromosomes relative to autosomes In organisms with XX/XY sex chromosomes could provide fundamental Insight Into the process of genome evolution. Here we report this ratio for 24 cynomolgus monkeys (Macaca fascicularis) originating In Indonesia, Malaysia, and the Philippines. The average X/A diversity ratios In these samples was 0.34 and 0.20 In the Indoneslan-Malayslan and Philippine populations, respectively, considerably lower than the null expectation of 0.75. A Philippine population supposed to derive from an ancestral population by founding events showed a significantly lower ratio than the parental population, suggesting a demographic effect for the reduction. Taking sex-specific mutation rate bias and demographic effect Into account, expected X/A diversity ratios generated by computer simulations roughly agreed with the observed data In the Intergenlc regions. In contrast, silent sites In genic regions on X chromosomes showed strong reduction In genetic diversity and the observed X/A diversity ratio In the genic regions cannot be explained by mutation rate bias and demography, Indicating that natural selection also reduces the level of polymorphism near genes. Whole-genome analysis of a female cynomolgus monkey also supported the notion of stronger reduction of genetic diversity near genes on the X chromosome.

(ProQuest: ... denotes formulae omitted.)

CONTRASTING the pattern of molecular evolution and genetic diversity on autosomes and sex chromosomes provides evolutionary insights into the organization of ge- nomes (reviewed in Vicoso and Charlesworth 2006). The different level of genetic diversity between autosomes and X chromosomes in organisms with mammalian-like sex de- termination systems (XX/XY system) is a debated issue (Andolfatto 2001 Vicoso and Charlesworth 2006; Hammer et al. 2008, 2010; Reinan et al. 2009). Although the ratio of X to autosomal genetic diversity (X/A diversity ratio) is expected to be 0.75 under "idealized" population genetic processes in the XX/XY system, many evolutionary factors influence the ratio. These factors include natural selection, demography, sex-biased reproductive success, sex-biased mi- gration rate, and male/female mutation rate differences (re- viewed in Caballero 1994; Vicoso and Charlesworth 2006). For example, natural selection (both positive and negative selection) could reduce genetic diversity on functional sites and linked neutral sites; the magnitude of the effect de- pends on many factors, such as effective population size, strength of selection (selection and dominance coefficients), and recombination rate (Charlesworth 2012). Those effects could be different between autosomes and the X chromo- some and potentially increase or decrease the X/A diversity ratio (Begun and Whitley 2000; Vicoso and Charlesworth 2009). Selection-free processes such as demography could also drastically change the ratio. Previous theoretical studies showed that the ratio would increase after a population ex- pansion and decrease after a population reduction or bottle- neck (Pool and Nielsen 2007; Pool and Nielsen 2008). Similarly, the ratio would also decrease when the mutation rate per generation is higher in males than in females, pre- sumably owing to more germ-line cell divisions in males than in females, an effect known as male-driven molecular evolution (Miyata et al. 1987). Because so many factors could bias the X/A diversity ratio, it is often challenging to find the actual cause of bias.

The estimates on the X/A genetic diversity ratios in humans have been conflicting among studies, crossing the boundary of the neutral expectation of 0.75, after control- ling mutation rate bias (Hammer et al. 2008; Bustamante and Ramachandran 2009; Reinan et al. 2009). In nonhuman primates, however, some studies have reported much lower ratios. For example, a recent genome-wide resequencing study in central chimpanzees (Pan troglodytes) found a ratio of near 0. …

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