Evaluating genomic signatures of “the large X‐effect” during complex speciation

Abstract

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.

Variation in hybrid gene expression: Implications for the evolution of genetic incompatibilities in interbreeding species

“…Although introgression within sympatry does not fully explain the observed results, our finding that the sympatric hybrid types (BMs and MBs) consistently differed could be accounted for by differential introgression of the X chromosome in sympatry (Presgraves, ). Differential movement of the X chromosome relative to introgression in the remainder of the genome could also possibly account, at least in part, for the exaggeration (or reduction) of BDMs in sympatric hybrids relative to allopatric hybrids.…”

Ancestral and neo‐sex chromosomes contribute to population divergence in a dioecious plant

“…These results are consistent with growing evidence in many systems that population divergence often proceeds despite on‐going gene flow. This “complex speciation” model implies that different genomic regions, including sex chromosomes, can contribute disproportionately to population differentiation throughout the process of divergence (Presgraves ). We also found evidence for elevated between‐population differentiation on the sex chromosomes compared with autosomes, consistent with observations from several animal taxa (reviewed in Presgraves ).…”

“…Analyses of genomic heterogeneity in divergence have often identified sex chromosomes as outliers of differentiation (Presgraves ). This finding is not unexpected: sex chromosomes have long been thought to be associated with speciation (Coyne and Orr 2004).…”

“…). Additionally, heterogeneous patterns of differentiation can be driven by local adaptation (Presgraves ). Because of these results, the broad generality of the large X pattern remains uncertain (Coyne ; Presgraves ), especially in plants in which dioecy and sex chromosomes have both evolved relatively recently from hermaphroditic ancestors.…”

Quantifying the relative contributions of the X chromosome, autosomes, and mitochondrial genome to local adaptation*

“…; Camus et al. ), while also raising questions about the scope of “faster‐X effects” in adaptive evolution (i.e., the extent to which X‐linked genes diverge more rapidly than autosomal genes during adaptation; Presgraves, , ; Meisel and Connallon ; Lasne et al. ; Charlesworth et al.…”