Anisogamy evolved with a reduced sex-determining region in volvocine green algae

Abstract

Male and female gametes differing in size—anisogamy—emerged independently from isogamous ancestors in various eukaryotic lineages, although genetic bases of this emergence are still unknown. Volvocine green algae are a model lineage for investigating the transition from isogamy to anisogamy. Here we focus on two closely related volvocine genera that bracket this transition—isogamous Yamagishiella and anisogamous Eudorina. We generated de novo nuclear genome assemblies of both sexes of Yamagishiella and Eudorina to identify the dimorphic sex-determining chromosomal region or mating-type locus (MT) from each. In contrast to the large (>1 Mb) and complex MT of oogamous Volvox, Yamagishiella and Eudorina MT are smaller (7–268 kb) and simpler with only two sex-limited genes—the minus/male-limited MID and the plus/female-limited FUS1. No prominently dimorphic gametologs were identified in either species. Thus, the first step to anisogamy in volvocine algae presumably occurred without an increase in MT size and complexity.

Algal Sex Determination and the Evolution of Anisogamy

“…A MID ortholog is found in the minus or male MT loci of all heterothallic volvocine algae identified to date (43,44,56,57,105), and MID has also now been identified in a homothallic volvocine species where its expression may be controlled epigenetically 145 Table 1). 4b).…”

“…A. Diagrams of volvocine SDRs or MDRs adapted from [57]. The heteromorphic regions are depicted in blue (MT-or male) and red (MT+ or female) for each species with co-linear flanking regions in solid black and dashed lines.…”

“…Some volvocine species have a second MT− or male MT gene, MTD1, whose C. reinhardtii ortholog contributes to minus gametic differentiation but is not essential for it(86) (Figure 4a). In C. reinhardtii, and in other volvocine genera where -N is cue for gametogenesis, MID expression is induced by -N (44,55,57,86) (Figure 3b). C. reinhardtii mid mutants have a pseudo plus phenotype where they differentiate and agglutinate as plus gametes but cannot complete fertilization due to absence of the FUS1 gene(Figure 4a), whose expression as a transgene can fully rescue fertility in a mid mutant.…”

Consequences of recombination for the evolution of the mating type locus inChlamydomonas reinhardtii

“…The MT locus of V. carteri, for instance, is five times 448 larger than C. reinhardtii MT, more differentiated, and also carries more sex-specific 449 genes (Ferris et al, 2010). Differentiation between the V. carteri MT alleles likely 450 occurred after the transition to anisogamy (Hiraide et al, 2013, Hamaji et al, 2018, 451 suggesting that selection for recombination suppression followed the appearance of 452 selective pressure on sex-specific traits. Thus, given our findings that gene conversion 453 is a strong predictor of both selection efficacy and differentiation levels across C.…”

“…Evidence of degeneration is restricted 463 to MT -limited genes in C. reinhardtii, which we show exhibit low diversity and less 464 effective selection. In addition to C. reinhardtii, other isogamous algae also show 465 very low levels of differentiation in shared regions (Hamaji et al, 2016(Hamaji et al, , 2018 Table S1: Field strains of C. reinhardtii used in this study. All strains were obtained from the Chlamydomonas Resource Center (chlamycollection.org).…”