Genome Diversity and Divergence in Drosophila mauritiana : Multiple Signatures of Faster X Evolution

Abstract

Drosophila mauritiana is an Indian Ocean island endemic species that diverged from its two sister species, Drosophila simulans and Drosophila sechellia, approximately 240,000 years ago. Multiple forms of incomplete reproductive isolation have evolved among these species, including sexual, gametic, ecological, and intrinsic postzygotic barriers, with crosses among all three species conforming to Haldane’s rule: F1 hybrid males are sterile and F1 hybrid females are fertile. Extensive genetic resources and the fertility of hybrid females have made D. mauritiana, in particular, an important model for speciation genetics. Analyses between D. mauritiana and both of its siblings have shown that the X chromosome makes a disproportionate contribution to hybrid male sterility. But why the X plays a special role in the evolution of hybrid sterility in these, and other, species remains an unsolved problem. To complement functional genetic analyses, we have investigated the population genomics of D. mauritiana, giving special attention to differences between the X and the autosomes. We present a de novo genome assembly of D. mauritiana annotated with RNAseq data and a whole-genome analysis of polymorphism and divergence from ten individuals. Our analyses show that, relative to the autosomes, the X chromosome has reduced nucleotide diversity but elevated nucleotide divergence; an excess of recurrent adaptive evolution at its protein-coding genes; an excess of recent, strong selective sweeps; and a large excess of satellite DNA. Interestingly, one of two centimorgan-scale selective sweeps on the D. mauritiana X chromosome spans a region containing two sex-ratio meiotic drive elements and a high concentration of satellite DNA. Furthermore, genes with roles in reproduction and chromosome biology are enriched among genes that have histories of recurrent adaptive protein evolution. Together, these genome-wide analyses suggest that genetic conflict and frequent positive natural selection on the X chromosome have shaped the molecular evolutionary history of D. mauritiana, refining our understanding of the possible causes of the large X-effect in speciation.

Genetics on the Fly: A Primer on theDrosophilaModel System

“…Owing to the abundance of new genetic and molecular tools, the field of speciation genetics is growing (reviewed in Presgraves 2010). Population genomic resources now exist for several species closely related to D. melanogaster, including D. simulans (Rogers et al 2014), D. mauritiana (Nolte et al 2013;Garrigan et al 2015), and D. yakuba (Rogers et al 2014) with several additional datasets on the way (http:// www.dpgp.org/1K_300genomes.html). Population-level data on transcriptomes (RNA sequence datasets) are also available for studying gene regulatory evolution and de novo genes (Zhao et al 2014).…”

Contrasting Levels of Molecular Evolution on the Mouse X Chromosome

“…Faster-X protein evolution has now been found across a broad range of taxa, including mammals (Hvilsom et al 2012;Veeramah et al 2014), birds (Mank et al 2007), flies (Begun et al 2007;Langley et al 2012;Garrigan et al 2014), and other insects (Jaquiery et al 2012;Sackton et al 2014). Both higher rates of adaptive substitutions (Kousathanas et al 2014) and relaxed constraint likely contribute to these patterns.…”

Neighboring genes for DNA-binding proteins rescue male sterility in Drosophila hybrids

“…Although genomic conflicts over sex chromosome transmission contribute significantly to the evolution of reproductive isolation (23,24,(26)(27)(28), the autosomes alone contain ∼40 genetic regions that contribute significantly to hybrid male sterility (29).…”