Three genomes in the algal genus Volvox 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 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.

Switching it up: algal insights into sexual transitions

“…Notably, while many of the female gametolog descendants were retained in the SDLR of V. africanus , no homologs of female sex-limited genes were retained, including the conserved FUS1 gene encoding a membrane-localized fertilization protein that was also lost in the V. carteri lineage. Importantly, as predicted from earlier work (Yamamoto et al 2017 ), V. africanus had a separate chromosomal region that contained a tandem array of MID genes and an unlinked autosomal region containing another conserved male/minus gene, MTD1 . Interestingly, three other autosomal regions had insertions of male-derived gametologs and one had a female gametolog.…”

“…Cartoons depict the two types of sexual individuals produced from V. africanus clones-male spheroids and monoicous spheroids containing eggs and sperm packets. This figure was based on previously published work (Umen and Coelho 2019;Yamamoto et al 2021) question of how male-specific or female-specific functions that evolved as sex chromosomes genes become resolved in a transition to homothallism? A recent study comparing the genomes of homothallic V. africanus to male and female SDRs of a heterothallic close relative, V. reticuliferus (~ 11 My divergence time), has begun to shed light on this question (Yamamoto et al 2021).…”

“…This figure was based on previously published work (Umen and Coelho 2019;Yamamoto et al 2021) question of how male-specific or female-specific functions that evolved as sex chromosomes genes become resolved in a transition to homothallism? A recent study comparing the genomes of homothallic V. africanus to male and female SDRs of a heterothallic close relative, V. reticuliferus (~ 11 My divergence time), has begun to shed light on this question (Yamamoto et al 2021). Although V. africanus no longer possesses sex chromosomes, it retained a chromosomal region that was very similar in size, gene content, and sequence characteristics to the V. reticuliferus female SDR, revealing a past history of this SD-like region (SDLR) as a female sex chromosome (Fig.…”

“…Cartoons depict the two types of sexual individuals produced from V. africanus clones—male spheroids and monoicous spheroids containing eggs and sperm packets. This figure was based on previously published work (Umen and Coelho 2019 ; Yamamoto et al 2021 ) …”

Evolutionary Genomics of Sex-Related Chromosomes at the Base of the Green Lineage

“…Recombination suppression may be stepwise and thus generate “evolutionary strata” of differentiation between the two mating types ( Hartmann et al [2021] for a review in Fungi). The consequence of recombination suppression are manifold ( Charlesworth and Charlesworth 2000 ; Charlesworth 2016 ) and may include a higher probability of fixation of deleterious mutations, massive rearrangements, which may be associated to lower gene density ( Yamamoto et al 2021 ), GC composition changes, as well as differential gene expression ( Ma et al 2020 ). GC composition results from the balance between mutation biases, selection, and GC-biased gene conversion ( Galtier et al 2001 ), a molecular process linked to recombination.…”