I believe that sex is one of the most beautiful, natural, wholesome things that money can buy.

–Steve Martin

Volvox, and the volvocine algae in general, are well known as a model system for the evolution of multicellularity and cellular differentiation, but they are also an outstanding model for the evolution of sex and mating types. Volvocine algae are facultatively sexual, with haploid vegetative colonies reproducing asexually through mitosis but occasionally entering a sexual cycle that usually results in a diploid, desiccation-resistant zygote or ‘spore.’ Most of the small colonial species and unicellular relatives are isogamous, that is, the gametes are of equal size. Nevertheless, each species has two self-incompatible mating types, usually designated as ‘plus’ and ‘minus.’ In some of the larger species, the gametes have diverged into a small, motile form that we call sperm and a large, often immotile form that we call eggs. Across the eukaryotic domain, it is gamete size, not form of genitalia, fancy plumage, or receding hairline, that define males and females.

The volvocine algae span a wide range of mating systems, making them a useful (and I think underutilized) system for comparative studies of the evolution of sex. As I’ve already mentioned, both isogamous (equal-sized gametes) and oogamous (sperm and eggs) species exist, and there is good reason to suspect that oogamy has evolved independently in two separate lineages:

Isogamy and oogamy (Kirk 2006. Curr. Biol., 16:R1028.)

Furthermore, among the oogamous species, some are heterothallic (i.e. they have genetic sex determination) and some homothallic (i.e. a single genotype can produce both males and females). Among the homothallic species, some are dioecious (i.e. produce separate male and female colonies), others monoecious (i.e. hermaphroditic colonies produce both sperm and eggs), and still others produce both hermaphroditic and male colonies (more on this in a future post). Some of these traits may even vary within species, although species delimitation has historically been so problematic that I wouldn’t bank on this.

Males and females have evolved many times independently from different groups of isogamous ancestors, for example in animals, plants, and various groups of multicellular algae. The genetics that determine maleness and femaleness are well understood in most of these groups, but their origins are much more mysterious. In fact, the volvocine algae are (as far as I know) the only taxonomic group in which we know which isogamous mating type evolved into males and which into females.

Yesterday’s first morning session focused on life cycles and included three talks on sexual reproduction in various volvocine species (the fourth talk, on phenotypic plasticity, I’ll address in a separate post). The session was introduced by Jim Umen from the Donald Danforth Plant Science Center, who emphasized the aspects common to all volvocine life cycles: asexual (vegetative) reproduction through mitosis, a sexual cycle induced species-specific signals, gametic interactions and eventual fusion generating a diploid zygospore, and meiosis and germination of the zygospore re-initiating the asexual phase of the life cycle.

The multiple fission cell cycle and sexual cycles of Chlamydomonas and Gonium (Umen & Olson 2012. Adv. Bot. Res. 64:185). During vegetative growth (A), Chlamydomonas cells may grow many fold in size; cells then divide multiple times to produce uniform-sized daughters (two rounds of cell division are shown in this panel). Gonium colonies (B) follow a similar growth and division pattern as Chlamydomonas, but the daughter cells remain attached to each other through cytoplasmic bridges and ECM. The Chlamydomonas sexual cycle (C) is induced by lack of nitrogen (−N) that causes cells to differentiate into gametes. Flagellar adhesion between gametes of opposite mating type precedes cell fusion to form a diploid zygote. Upon germination, four meiotic progeny are produced that can re-enter the vegetative cycle. In Gonium −N also triggers gametogenesis that involves colony dissolution into unicellular gametes. Post-meiotic Gonium progeny are single cells that produce a new vegetative colony after their first passage through the cell cycle.

Hiroko Kawai-Toyooka, from the University of Tokyo, described the isolation of mating structures from Gonium pectorale, a small colonial volvocine alga. Like Chlamydomonas, Gonium is isogamous, and its gametes have cellular protrusions that function in gamete fusion. Isolation of these structures is a first step toward characterizing proteins involved in gamete fusion, and it will be interesting to learn how conserved these proteins are across various volvocine species.

Takashi Hamaji, from the Donald Danforth Plant Science Center in St. Louis, presented results of a global gene expression analysis of Volvox carteri. In both male and female strains, Dr. Hamaji isolated and sequenced RNA from an impressive 64 time points distributed throughout the asexual and sexual life cycles. Genes showing both male-specific and female-specific expression were identified from the RNA-Seq data, providing clues to the genetic basis of the sexual cycle.

Sa Geng, also from the Danforth Center, investigated the role of the MID gene, which determines isogamous mating type in Chlamydomonas, in both mating type and sex determination in colonial species of volvocine algae. Dr. Geng’s previous work showed that MID evolved from an ancestral role in mating type determination to a similar role in the oogamous species Volvox carteri. By creating transgenic strains expressing MID genes from other species, Dr. Geng tested both when MID acquired the ability to control sperm and egg development and whether MID genes from oogamous species could determine mating type in Chlamydomonas. His results suggest that changes in gene regulatory networks, rather than in the MID gene itself, underlay the evolution of males and females in the volvocine algae.

The outrageous variability of sexual systems in the volvocine algae makes them a valuable system for comparative studies with the potential to bear on some of the toughest problems in evolutionary biology. As with any model system, it is difficult to say how general and how system-specific any results are, but generalizations have to begin with individual data points, and the volvocine algae are emerging as one of the best understood examples of an evolutionary transition from isogamous to oogamous sexual reproduction. As other systems catch up, it will be interesting to see how much of what we have learned from the volvocines turns out to be common to such transitions.