Birth of a W sex chromosome by horizontal transfer ofWolbachiabacterial symbiont genome

Abstract

Sex determination is a fundamental developmental pathway governing male and female differentiation, with profound implications for morphology, reproductive strategies, and behavior. In animals, sex differences between males and females are generally determined by genetic factors carried by sex chromosomes. Sex chromosomes are remarkably variable in origin and can differ even between closely related species, indicating that transitions occur frequently and independently in different groups of organisms. The evolutionary causes underlying sex chromosome turnover are poorly understood, however. Here we provide evidence indicating that Wolbachia bacterial endosymbionts triggered the evolution of new sex chromosomes in the common pillbug Armadillidium vulgare. We identified a 3-Mb insert of a feminizing Wolbachia genome that was recently transferred into the pillbug nuclear genome. The Wolbachia insert shows perfect linkage to the female sex, occurs in a male genetic background (i.e., lacking the ancestral W female sex chromosome), and is hemizygous. Our results support the conclusion that the Wolbachia insert is now acting as a female sex-determining region in pillbugs, and that the chromosome carrying the insert is a new W sex chromosome. Thus, bacteria-to-animal horizontal genome transfer represents a remarkable mechanism underpinning the birth of sex chromosomes. We conclude that sex ratio distorters, such as Wolbachia endosymbionts, can be powerful agents of evolutionary transitions in sex determination systems in animals.sex chromosome | horizontal transfer | Wolbachia | endosymbiont | isopod crustacean

How to identify sex chromosomes and their turnover

“…Endosymbionts can have a similar impact, as illustrated by the Wolbachia feminizing element in populations of woodlice (Cordaux, Bouchon, & Grève, ). Increasing numbers of theoretical models outline the scenarios in which we might expect sex ratio selection to drive the evolution of new sex chromosome systems (Kozielska, Weissing, Beukeboom, & Pen, ; Úbeda, Patten, & Wild, ) and there is growing support from a few taxa (Badawi, Moumen, Giraud, Grève, & Cordaux, ; Becking et al, ; Chebbi et al, ; Cordaux et al, ; Cordaux & Gilbert, ; Leclercq et al, ; Miura, ). Similarly, a recent study outlined the role of haploid selection via gametic competition and meiotic drive in increasing the lability of sex determination systems (Scott et al, ).…”

Population genetics of sexual conflict in the genomic era

“…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.…”

A newly evolved W(olbachia) sex chromosome in pillbug!

“…Although the Wolbachia-derived gene(s) that became sex-determining gene(s) remain to be identified among many possible candidates, the genomic and genetic evidence are clear that this Wolbachia insertion is determining sex in this pillbug strain. Leclerq et al [5] also found that although this insertion is quite recent, many structural changes (rearrangements, duplications) have occurred compared to the wVulC genome, which study will probably help understand which bacterial gene(s) have retained a function in the nucleus of the pillbug. Also, in the future, it will be interesting to understand how and why exactly the nuclear inserted Wolbachia rose in frequency in the pillbug population and how the cytoplasmic Wolbachia was lost, and to tease apart the roles of selection and drift in this event.…”

“…Several models have been developed to explain this pattern but empirical data are lacking and the causes of the fast sex chromosome turn over remain mysterious [2][3][4]. Leclerq et al [5] in a paper that just came out in PNAS have focused on one possible explanation: Wolbachia. This widespread intracellular symbiont of arthropods can manipulate its host reproduction in a number of ways, often by biasing the allocation of resources toward females, the transmitting sex.…”

“…Intriguingly, studies from natural populations also report that some females are devoid both of Wolbachia and the ancestral W chromosome, suggesting the existence of new female determining nuclear factor, the hypothetical "f element". Leclerq et al [5] found the f element and decrypted its origin. By sequencing the genome of a strain carrying the putative f element, they found that a nearly complete wVulC genome got inserted in the nuclear genome and that the chromosome carrying the insertion has effectively become a new W chromosome.…”