Transition from Environmental to Partial Genetic Sex Determination in Daphnia through the Evolution of a Female-Determining Incipient W Chromosome.

Céline M.O Reisser,Marinela Dukič,Virginie Thuillier,Dominique Fasel,Yan Galimov,Christoph R Haag,Evelin Hürlimann,Cathy Haag-Liautard

doi:10.1093/molbev/msw251

Abstract

Sex chromosomes can evolve during the evolution of genetic sex determination (GSD) from environmental sex determination (ESD). Despite theoretical attention, early mechanisms involved in the transition from ESD to GSD have yet to be studied in nature. No mixed ESD-GSD animal species have been reported, except for some species of Daphnia, small freshwater crustaceans in which sex is usually determined solely by the environment, but in which a dominant female sex-determining locus is present in some populations. This locus follows Mendelian single-locus inheritance, but has otherwise not been characterized genetically. We now show that the sex-determining genomic region maps to the same low-recombining peri-centromeric region of linkage group 3 (LG3) in three highly divergent populations of D. magna, and spans 3.6 Mb. Despite low levels of recombination, the associated region contains signs of historical recombination, suggesting a role for selection acting on several genes thereby maintaining linkage disequilibrium among the 36 associated SNPs. The region carries numerous genes involved in sex differentiation in other taxa, including transformer2 and sox9. Taken together, the region determining the genetic females shows characteristics of a sex-related supergene, suggesting that LG3 is potentially an incipient W chromosome despite the lack of significant additional restriction of recombination between Z and W. The occurrence of the female-determining locus in a pre-existing low recombining region illustrates one possible form of recombination suppression in sex chromosomes. D. magna is a promising model for studying the evolutionary transitions from ESD to GSD and early sex chromosome evolution.

Highlights

Sex chromosomes have evolved independently multiple times in many taxa (Miura 2008; Pokorna and Kratochvıl 2009; Stock et al 2011; Cheng et al 2013; The Tree of Sex Consortium 2014)
Our results suggest that the NMP phenotype is determined by a single, large genomic region located on linkage group 3 (LG3)
The few significantly linked singlenucleotide polymorphism (SNP) on other linkage groups may be in linkage disequilibrium with the major region on LG3, maintained by pleiotropic effects

Summary

Introduction

Sex chromosomes have evolved independently multiple times in many taxa (Miura 2008; Pokorna and Kratochvıl 2009; Stock et al 2011; Cheng et al 2013; The Tree of Sex Consortium 2014). Separate sexes may evolve from hermaphroditism, most likely through a male-sterility (i.e., female determining) mutation creating a breeding system called gynodioecy, with genetic females co-occurring with functional hermaphrodites. Additional mutations in genes linked to the sexdetermining locus may be favored if their effects are sexually antagonistic (i.e. have opposite effects in the two sexes; Rice 1987; Ellegren 2011). Closer linkage will be favored in this genomic region (Bull 1983), which may lead to suppression of recombination. This may result in a system with “proto-sex chromosomes” carrying linked genes that determine both sexes genetically (with male and female determining mutations on opposite homologs)

Methods

Results

Conclusion