Diversity and evolution of sex determination systems in terrestrial isopods

Abstract

Sex determination systems are highly variable in many taxa, sometimes even between closely related species. Yet the number and direction of transitions between these systems have seldom been characterized, and the underlying mechanisms are still poorly understood. Here we generated transcriptomes for 19 species of terrestrial isopod crustaceans, many of which are infected by Wolbachia bacterial endosymbionts. Using 88 single-copy orthologous genes, we reconstructed a fully resolved and dated phylogeny of terrestrial isopods. An original approach involving crossings of sex-reversed individuals allowed us to characterize the heterogametic systems of five species (one XY/XX and four ZW/ZZ). Mapping of these and previously known heterogametic systems onto the terrestrial isopod phylogeny revealed between 3 and 13 transitions of sex determination systems during the evolution of these taxa, most frequently from female to male heterogamety. Our results support that WW individuals are viable in many species, suggesting sex chromosomes are at an incipient stage of their evolution. Together, these data are consistent with the hypothesis that nucleo-cytoplasmic conflicts generated by Wolbachia endosymbionts triggered recurrent turnovers of sex determination systems in terrestrial isopods. They further establish terrestrial isopods as a model to study evolutionary transitions in sex determination systems and pave the way to molecularly characterize these systems.

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, ).…”

Sex chromosome turnovers and genetic drift: a simulation study

“…Thanks to recent advances in genomic technologies, sex chromosome systems are now characterized across a wide range of nonmodel organisms, revealing that many clades experience frequent sex chromosome turnovers, whereby an ‘emergent’ mutant sex determiner replaces the ‘resident’ sex determiner at the top of the sex‐determining cascade. This is the case for instance in fishes (Mank & Avise, ), reptiles (Ezaz et al ., ), amphibians (Miura, ; Dufresnes et al ., ; Furman & Evans, ), Diptera (Vicoso & Bachtrog, ), isopods (Becking et al ., ) and Salicaceae (Muyle et al ., ).…”

Sex chromosomes control vertical transmission of feminizing Wolbachia symbionts in an isopod

“…However, unlike A. vulgare , chromosomal sex determination follows XY/XX heterogamety in A. nasatum [20, 35]. This result was established using an original strategy consisting of experimentally reversing young genetic females into phenotypic males, crossing them with their sisters and analyzing sex ratios of the resulting progenies [20, 35]. Here, based on whole-genome sequencing, pedigree analyses and simulations, we show that Wolbachia endosymbionts can spread in A. nasatum populations because A. nasatum sex chromosomes are genetically highly similar and YY males and females are both viable and fertile.…”

“…Here, we investigated the interplay between sex chromosomes and Wolbachia symbionts in Armadillidium nasatum , a terrestrial isopod species related to A. vulgare [20]. Analogous to A. vulgare , a feminizing Wolbachia strain ( w Nas) is naturally present in A. nasatum [21,35,36].…”

“…Analogous to A. vulgare , a feminizing Wolbachia strain ( w Nas) is naturally present in A. nasatum [21,35,36]. However, unlike A. vulgare , chromosomal sex determination follows XY/XX heterogamety in A. nasatum [20, 35]. This result was established using an original strategy consisting of experimentally reversing young genetic females into phenotypic males, crossing them with their sisters and analyzing sex ratios of the resulting progenies [20, 35].…”