Speciation through evolution of sex-linked genes

Abstract

Identification of genes involved in reproductive isolation opens novel ways to investigate links between stages of the speciation process. Are the genes coding for ecological adaptations and sexual isolation the same that eventually lead to hybrid sterility and inviability? We review the role of sex-linked genes at different stages of speciation based on four main differences between sex chromosomes and autosomes; (1) relative speed of evolution, (2) non-random accumulation of genes, (3) exposure of incompatible recessive genes in hybrids and (4) recombination rate. At early stages of population divergence ecological differences appear mainly determined by autosomal genes, but fastevolving sex-linked genes are likely to play an important role for the evolution of sexual isolation by coding for traits with sex-specific fitness effects (for example, primary and secondary sexual traits). Empirical evidence supports this expectation but mainly in female-heterogametic taxa. By contrast, there is clear evidence for both strong X-and Z-linkage of hybrid sterility and inviability at later stages of speciation. Hence genes coding for sexual isolation traits are more likely to eventually cause hybrid sterility when they are sex-linked. We conclude that the link between sexual isolation and evolution of hybrid sterility is more intuitive in male-heterogametic taxa because recessive sexually antagonistic genes are expected to quickly accumulate on the X-chromosome. However, the broader range of sexual traits that are expected to accumulate on the Z-chromosome may facilitate adaptive speciation in female-heterogametic species by allowing male signals and female preferences to remain in linkage disequilibrium despite periods of gene flow.

Patterns of genetic diversity and differentiation in resistance gene clusters of two hybridizing European Populus species

“…However, contrary to expectations for both sex determination genes and R-genes from other species (Bomblies and Weigel 2007;Qvarnström and Bailey 2009;Ellegren 2009), chromosome XIX of European poplar species exhibits unusually low levels of species differentiation (Macaya-Sanz et al 2011;Stölting et al 2013; this study). More extensive work based on high-throughput genotyping-by-sequencing and whole genome resequencing is currently underway to clarify the precise roles of recurrent gene flow and shared selection pressures in generating the conspicuous patterns of allele sharing and LD observed in this enigmatic genome region of poplar.…”

“…Reproductive isolation was shown to result from a great number of different preand postzygotic mechanisms in animals and plants, including sexual, genetic, and ecological barriers (Smadja and Butlin 2011). In some animal species, sex determination regions host species isolation genes (reviewed by Qvarnström and Bailey 2009;Ellegren 2009). In plants, resistance genes have been put forward for their potential role in the origin and maintenance of reproductive barriers through hybrid necrosis (Bomblies and Weigel 2007;Bomblies 2009).…”

Community assembly inNothobranchiusannual fishes: Nested patterns, environmental niche and biogeographic history

“…However, Nothobranchius genomes are evolving at a fast rate (Reichwald et al., 2015; Valenzano et al., 2015), with intra‐specific differentiation in the sex determination system in N. furzeri (Valenzano et al., 2015). Divergence in sex determination systems and sex‐linked genes is known to drive speciation across several taxa (Kitano et al., 2009; Qvarnström & Bailey, 2009). Interestingly, species of the R‐clade differ cytogenetically (Shidlovskiy et al., 2010), and it is possible that a combination of allopatric diversification and major cytogenetic incompatibilities during secondary sympatry may promote speciation at least in some Nothobranchius lineages.…”

The genetic architecture of sexually selected traits in two natural populations of Drosophila montana

“…The low X coverage would be particularly unfortunate if there is a large X effect, that is if the X is disproportionately influencing reproductive isolation (Presgraves, 2008) or genes under sexual selection (Qvarnstrom and Bailey, 2009;Dean and Mank, 2014), which may have further hindered our ability to detect segregating genetic variation for these traits.…”