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.

Figure 1.—

N_e of aDNA, xDNA, mtDNA, and yDNA as a function of (A) sex ratio skew and (B) the probability of female dispersal. In B, a finite island model of subdivided populations of constant size is assumed with a population size of 10,000 individuals, 10 subpopulations, and a male probability of migration equal to 0.1.

Figure 2.—

Likelihood surfaces of N_e-xDNA/N_e-aDNA, N_e-yDNA/N_e-aDNA, and N_e-mtDNA/N_e-aDNA, ratios. A solid arrowhead indicates the ideal expectation with an equal number of males and females for N_e-yDNA/N_e-aDNA, and N_e-mtDNA/N_e-aDNA (inheritance = 0.25) and a shaded arrowhead indicates the expectation for N_e-xDNA/N_e-aDNA (inheritance = 0.75). Note that the most likely N_e-xDNA/N_e-aDNA ratio is lower than the ideal expectation with an equal number of females and males and also lower than the predictions from the demographic models we examined. However, 95% confidence limits, which are the parameter values with <2 ln(L) units lower than the maximum likelihood value (i.e. above the dashed line), include both of these expectations.

Figure 3.—

Scaling factors for N_e-xDNA:N_e-aDNA, N_e-yDNA:N_e-aDNA, and N_e-mtDNA:N_e-aDNA (black lines; left y-axis) under a demographic model with (A) skewed sex ratio and (B) sex-biased dispersal, and likelihood (red lines; right y-axis) of M. nemestrina polymorphism and divergence data under each model given these scaling factors. The scaling factors were calculated according to model expectations described in File S1. Model B assumes male migration is 0.1 and a population size of 10,000 individuals divided into 10 equally sized subpopulations. Red arrowheads indicate the likelihood of ideal expectation with no sex ratio skew in A and no sex-bias in dispersal in B. A dotted red line indicates the 95% confidence interval 2lnL units below the maximum likelihood value.

Figure 4.—

Posterior distributions of parameters of (A) 4Neμ of macaque monkey populations on Borneo (θ_B), the Sulawesi species M. tonkeana (θ_S), the ancestor of these populations before divergence (θ_A), (B) divergence time (T), and for the asymmetric migration model, (C) migration from Borneo to Sulawesi (m_BS), and from Sulawesi to Borneo (m_SB).

Figure 5.—

TBL1X is not monophyletic in Sulawesi macaques. A well-supported clade with a synapomorphic SNP and a synapomorphic insertion/deletion (indel) occurs on Sulawesi and on Borneo. One TBLIX lineage was sampled on northwest Sulawesi in M. hecki and M. nigrescens and in M. nemestrina from northeast, west, and south Borneo. The other lineage was sampled in several other Sulawesi macaque species and in M. nemestrina from west and south Borneo. Posterior probabilities ≥100 or 95% are indicated by circles on nodes that are filled or half filled, respectively. The posterior probability of Sulawesi paraphyly, which does not take into account additional support of the insertion/deletion, is 99%. This indicates that the chance that these linked mutations arose independently on either side of the Makassar Strait is remote. For female samples, each allele is indicated with an “a” or a “b” following the name. Scale bars indicate the number of substitutions per site; sample information is listed in File S1.