Convergent recombination suppression suggests role of sexual selection in guppy sex chromosome formation

Abstract

Sex chromosomes evolve once recombination is halted between a homologous pair of chromosomes. The dominant model of sex chromosome evolution posits that recombination is suppressed between emerging X and Y chromosomes in order to resolve sexual conflict. Here we test this model using whole genome and transcriptome resequencing data in the guppy, a model for sexual selection with many Y-linked colour traits. We show that although the nascent Y chromosome encompasses nearly half of the linkage group, there has been no perceptible degradation of Y chromosome gene content or activity. Using replicate wild populations with differing levels of sexually antagonistic selection for colour, we also show that sexual selection leads to greater expansion of the non-recombining region and increased Y chromosome divergence. These results provide empirical support for longstanding models of sex chromosome catalysis, and suggest an important role for sexual selection and sexual conflict in genome evolution.

Population genetics of sexual conflict in the genomic era

“…Data from studies in guppies (Poecilia reticulata) 27 and sticklebacks 66 are consistent with the theoretical prediction that recombination between the X and Y chromosomes is selected against in order to maintain male-benefit alleles on the Y chromosome [69][70][71][72] , thereby limiting their inheritance to males. In effect, male-specific genetic architecture is created through inheritance 27,66 of the Y chromosome, and sexual conflict is resolved because these alleles are simply never present in females. This process is not limited to male heterogametic species, as a similar effect has been shown in a female heterogametic cichlid, in which the formation of the W chromosome resolved sexual conflict over color 68 .…”

“…Sex chromosomes are the product of recombination suppression between the X and Y (or Z and W) chromosomes 65 , and there is increasing evidence that this process occurs in order to resolve sexual conflict 27,[66][67][68] . Data from studies in guppies (Poecilia reticulata) 27 and sticklebacks 66 are consistent with the theoretical prediction that recombination between the X and Y chromosomes is selected against in order to maintain male-benefit alleles on the Y chromosome [69][70][71][72] , thereby limiting their inheritance to males.…”

“…However, more recent studies point to the potential for sexual conflict over viability or survival, where an allele increases the likelihood that one sex will live long enough to reproduce at some cost to the other 17,18, 25 . Published [25][26][27][28] and preliminary 29 studies have also sparked new debate, for example, about how often and how quickly sexual conflict can be resolved.…”

Mapping Genomic Scaffolds to Chromosomes Using Laser Capture Microdissection in Application to Hawaiian Picture-Winged Drosophila

“…Early studies of the faster-X evolution in coding sequences of Drosophila species led to contradictory results [Betancourt et al, 2002;Thornton and Long, 2002;Thornton et al, 2006], but increasingly more studies tend to support this phenomenon [Charlesworth and Campos, 2014;Veeramah et al, 2014]. Newer studies also include a wider taxonomical spectrum, and include human, mouse, and birds [Kousathanas et al, 2014;Wang et al, 2014;Dean et al, 2015;Wright et al, 2017]. In addition to sequence divergence, divergent gene expression patterns in Drosophila and mammals are also pronounced among Xlinked genes [Hu et al, 2013;Kousathanas et al, 2014].…”

How to identify sex chromosomes and their turnover

“…Despite the growing awareness that sex chromosomes have evolved independently many times throughout eukaryotes, our understanding of the processes driving the formation and turnover of new sex chromosome systems is limited and many unanswered questions remain. A large body of theoretical work outlines predictions for when and why sex chromosome transitions occur (Beukeboom & Perrin, ), including genetic drift (Bull & Charnov, ; Saunders, Neuenschwander, & Perrin, ), mutation load on the sex‐limited chromosomes (Blaser, Grossen, Neuenschwander, & Perrin, ; Blaser, Neuenschwander, & Perrin, ), selection on sex ratio (Jaenike, ; Werren & Beukeboom, ) and sexually antagonistic selection (van Doorn & Kirkpatrick, , ), yet attempts to empirically test these have been restricted to a few clades (Blackmon & Demuth, ; Jeffries et al, ; Kitano & Peichel, ; Wright et al, ). Identifying the evolutionary and genomic mechanisms predicted to drive sex chromosome turnover is a major priority, which in turn will shed light on why sex determination is labile in some taxa and not in others.…”