Evaluating genomic signatures of "the large X-effect" during complex speciation.

The ubiquity of the "two rules of speciation"-Haldane's rule and the large X-effect-implies a general, special role for sex chromosomes in the evolution of intrinsic postzygotic reproductive isolation. The recent proliferation of genome-scale analyses has revealed two further general observations: (a) complex speciation involving some form of gene flow is not uncommon, and (b) sex chromosomes in male- and in female-heterogametic taxa tend to show elevated differentiation relative to autosomes. Together, these observations are consistent with speciation histories in which population genetic differentiation at autosomal loci is reduced by gene flow while natural selection against hybrid incompatibilities renders sex chromosomes relatively refractory to gene flow. Here, I summarize multilocus population genetic and population genomic evidence for greater differentiation on the X (or Z) vs. the autosomes and consider the possible causes. I review common population genetic circumstances involving no selection and/or no interspecific gene flow that are nevertheless expected to elevate differentiation on sex chromosomes relative to autosomes. I then review theory for why large X-effects exist for hybrid incompatibilities and, more generally, for loci mediating local adaptation. The observed levels of sex chromosome vs. autosomal differentiation, in many cases, appear consistent with simple explanations requiring neither large X-effects nor gene flow. Discerning signatures of large X-effects during complex speciation will therefore require analyses that go beyond chromosome-scale summaries of population genetic differentiation, explicitly test for differential introgression, and/or integrate experimental genetic data.