Human evolution: Sex-specific contributions to genome variation

Molecular Ecology, 2012

In the human species, the two uniparental genetic systems (mitochondrial DNA and Y chromosome) exhibit contrasting diversity patterns. It has been proposed that sex-specific behaviours, and in particular differences in migration rate between men and women, may explain these differences. The availability of high-density genomic data and the comparison of genetic patterns on autosomal and sex chromosomes at global and local scales allow a reassessment of the extent to which sex-specific behaviours shape our genome. In this article, we first review studies comparing the genetic patterns at uniparental and biparental genetic systems and assess the extent to which sex-specific migration processes explain the differences between these genetic systems. We show that differences between male and female migration rates matter, but that they are certainly not the only contributing factor. In particular, differences in effective population size between men and women are also likely to account for these differences. Then, we present and discuss three anthropological processes that may explain sex-specific differences in effective population size and thus human genomic variation: (i) variance in reproductive success arising from, for example, polygyny; (ii) descent rules; and (iii) transmission of reproductive success.

Constellations, 2010

Two central views about biology remain deeply entrenched in popular thought. The first is a picture of evolution. This is a set of ideas that reached their canonical form in the midtwentieth century, as the so-called ���New Synthesis��� of Darwinism and Mendelism, a version of which has become widely known due to the exceptional popularizing talents of Richard Dawkins. This is the view that evolution largely consists in small changes to genes, or to the human genome, which because of a small but incrementally advantageous ...

PLoS Genet, 2008

Comparisons of levels of variability on the autosomes and X chromosome can be used to test hypotheses about factors influencing patterns of genomic variation. While a tremendous amount of nucleotide sequence data from across the genome is now available for multiple human populations, there has been no systematic effort to examine relative levels of neutral polymorphism on the X chromosome versus autosomes. We analyzed ,210 kb of DNA sequencing data representing 40 independent noncoding regions on the autosomes and X chromosome from each of 90 humans from six geographically diverse populations. We correct for differences in mutation rates between males and females by considering the ratio of within-human diversity to human-orangutan divergence. We find that relative levels of genetic variation are higher than expected on the X chromosome in all six human populations. We test a number of alternative hypotheses to explain the excess polymorphism on the X chromosome, including models of background selection, changes in population size, and sex-specific migration in a structured population. While each of these processes may have a small effect on the relative ratio of X-linked to autosomal diversity, our results point to a systematic difference between the sexes in the variance in reproductive success; namely, the widespread effects of polygyny in human populations. We conclude that factors leading to a lower male versus female effective population size must be considered as important demographic variables in efforts to construct models of human demographic history and for understanding the forces shaping patterns of human genomic variability.

Nature Genetics, 2004

Science, 2013

The Y chromosome and the mitochondrial genome (mtDNA) have been used to estimate when the common patrilineal and matrilineal ancestors of humans lived. We sequenced the genomes of 69 males from nine populations, including two in which we find basal branches of the Y chromosome tree. We identify ancient phylogenetic structure within African haplogroups and resolve a longstanding ambiguity deep within the tree. Applying equivalent methodologies to the Y and mtDNA, we estimate the time to the most recent common ancestor (T MRCA ) of the Y chromosome to be 120-156 thousand years and the mtDNA T MRCA to be 99-148 ky. Our findings suggest that, contrary to prior claims, male lineages do not coalesce significantly more recently than female lineages.

The increasing availability of large-scale genetic datasets has made it possible to ask detailed questions about the structure of human genetic diversity, and what that structure can teach us about human demographic history. Global, multi-locus analyses have suggested that human genetic diversity may fall into clusters that correspond approximately to continental origin. Detailed comparisons of mitochondrial DNA and the Y chromosome have revealed a history of sex-biased migration patterns that can vary widely across human populations. These patterns can be understood, however, when we incorporate our knowledge of local histories and cultural practices into our genetic analyses.

Evolutionary Anthropology, 1996

Nature, 2002

Evolution, 2004

We show that a sex difference in the opportunity for selection results in sex differences in the strength of random genetic drift and thus creates different patterns of genetic diversity for maternally and paternally inherited haploid genes. We derive the effective population size N e for a male-limited or female-limited haploid gene in terms of I, the ''opportunity for selection'' or the variance in relative fitness. Because the variance in relative fitness of males can be an order of magnitude larger than that of females, the N e is much smaller for males than it is for females. We derive both nonequilibrium and equilibrium expressions for F ST in terms of I and show how the portion of I owing to sexual selection, I mates , that is, the variation among males in mate numbers, is a simple function of the F's for cytoplasmic (female inherited) and Y-linked (male inherited) genes. Because multiple, transgenerational data are lacking to apply the nonequilibrium expression, we apply only the equilibrium model to published data on Y chromosome and mitochondrial sequence divergence in Homo sapiens to quantify the opportunity for sexual selection. The estimate suggests that sexual selection in humans represents a minimum of 54.8% of total selection, supporting Darwin's proposal that sexual selection has played a significant role in human evolution and the recent proposal regarding a shift from polygamy to monogamy in humans.

Molecular Biology and Evolution, 1998

We surveyed nine diallelic polymorphic sites on the Y chromosomes of 1,544 individuals from Africa, Asia, Europe, Oceania, and the New World. Phylogenetic analyses of these nine sites resulted in a tree for 10 distinct Y haplotypes with a coalescence time of ϳ150,000 years. The 10 haplotypes were unevenly distributed among human populations: 5 were restricted to a particular continent, 2 were shared between Africa and Europe, 1 was present only in the Old World, and 2 were found in all geographic regions surveyed. The ancestral haplotype was limited to African populations. Random permutation procedures revealed statistically significant patterns of geographical structuring of this paternal genetic variation. The results of a nested cladistic analysis indicated that these geographical associations arose through a combination of processes, including restricted, recurrent gene flow (isolation by distance) and range expansions. We inferred that one of the oldest events in the nested cladistic analysis was a range expansion out of Africa which resulted in the complete replacement of Y chromosomes throughout the Old World, a finding consistent with many versions of the Out of Africa Replacement Model. A second and more recent range expansion brought Asian Y chromosomes back to Africa without replacing the indigenous African male gene pool. Thus, the previously observed high levels of Y chromosomal genetic diversity in Africa may be due in part to bidirectional population movements. Finally, a comparison of our results with those from nested cladistic analyses of human mtDNA and ␤-globin data revealed different patterns of inferences for males and females concerning the relative roles of population history (range expansions) and population structure (recurrent gene flow), thereby adding a new sex-specific component to models of human evolution.