Three genomes in the algal genus <i>Volvox</i> reveal the fate of a haploid sex-determining region after a transition to homothallism.

Abstract

Transitions between separate sexes (dioecy) and other mating systems are common across eukaryotes. Here, we study a change in a haploid dioecious green algal species with male- and female-determining chromosomes (U and V). The genus <i>Volvox</i> is an oogamous (with large, immotile female gametes and small, motile male gametes) and includes both heterothallic species (with distinct male and female genotypes, associated with a mating-type system that prevents fusion of gametes of the same sex) and homothallic species (bisexual, with the ability to self-fertilize). We date the origin of an expanded sex-determining region (SDR) in <i>Volvox</i> to at least 75 Mya, suggesting that homothallism represents a breakdown of dioecy (heterothallism). We investigated the involvement of the SDR of the U and V chromosomes in this transition. Using de novo whole-genome sequences, we identified a heteromorphic SDR of ca 1 Mbp in male and female genotypes of the heterothallic species <i>Volvox reticuliferus</i> and a homologous region (SDLR) in the closely related homothallic species <i>Volvox africanus</i>, which retained several different hallmark features of an SDR. The <i>V. africanus</i> SDLR includes a large region resembling the female SDR of the presumptive heterothallic ancestor, whereas most genes from the male SDR are absent. However, we found a multicopy array of the male-determining gene, <i>MID</i>, in a different genomic location from the SDLR. Thus, in <i>V. africanus</i>, an ancestrally female genotype may have acquired <i>MID</i> and thereby gained male traits.