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

Significance Evolutionary transitions between species with separate sexes and species in which individuals have both sex functions have wide-ranging biological implications. It is largely unknown how such transitions occur in systems with haploid male- and female-determining chromosomes in algae and bryophytes. We investigated such a transition in the algal genus Volvox by making whole-genome sequences of two closely related species, one of which is heterothallic (with distinct males and females) and the other homothallic (with only bisexual, self-compatible individuals). The heterothallic species harbors a sex-determining region (SDR), while the homothallic species retains a nearly intact female-derived SDR-like region and separate regions containing key male genes. Thus, an ancestral female has probably become homothallic by acquiring genes that confer male functions.
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 Volvox 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 Volvox 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 Volvox reticuliferus and a homologous region (SDLR) in the closely related homothallic species Volvox africanus, which retained several different hallmark features of an SDR. The V. africanus 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, MID, in a different genomic location from the SDLR. Thus, in V. africanus, an ancestrally female genotype may have acquired MID and thereby gained male traits.