Origins of the sexes: Eudorina and Yamagishiella

Volvox and the volvocine algae have long been a model system for understanding the evolution of multicellularity and cellular differentiation, but more recently they’ve emerged as an important model for the evolution of males and females. Sperm-producing males and egg-producing females have evolved independently in most multicellular lineages, so understanding how and why this happens is crucial for understanding the evolution of complex life.

It’s a near certainty that the unicellular ancestors from which animals, plants, fungi, seaweeds, and other complex multicellular organisms evolved were isogamous. In other words, they were capable of sexual reproduction, but the gametes that fused to form a zygote were the same size (“iso” – equal; “gamous” – gametes). In each of these lineages, large and small gametes evolved, resulting in a condition referred to as anisogamy (unequal gametes).

One really interesting thing about anisogamy is that unlike other forms of cellular differentiation, which result from non-genetic differences, the differences between sperm-producing males and egg-producing females are often genetically controlled. The most familiar way this happens is through sex chromosomes, such as the XY system in most mammals and the ZW system in birds, but there are lots of variations on this theme (check out the duck-billed platypus for an odd example).

Last month Takashi Hamaji and colleagues reported new results related to the evolution of anisogamy in the volvocine algae. The article, in Communications Biology, describes the genetic basis of sex (or mating type) determination in two volvocine species, isogamous Yamagishiella and anisogamous Eudorina. Apart from this difference in gametes, Yamagishiella and Eudorina are otherwise very similar:

Hamaji et al. 2018 Fig. 3

Figure 3A&B from Hamaji et al. 2018. Sex induction and associated gene expression alternations in isogamous Y. unicocca and anisogamous Eudorina sp. a, b Asexual and sex-induced individuals of opposite sexes of Y. unicocca (plus/minus) (a) and Eudorina sp. (female/male) (b). Mating reactions (mixed, right panels) occurred after mixing induced cultures of the two sexes (middle panels). In Y. unicocca (a), clumping of the colonies and release of single-celled isogametes (arrowheads) were observed 1 h after mixing. In Eudorina sp. (b), sex induction treatment resulted in the formation of sperm packets and the packet dissociated into individual sperm that penetrated into a female colony (arrowheads) within 16 h after mixing. Scale bars, 20 µm.

Dr. Hamaji’s previous work showed that the mating-type loci of isogamous, colonial Gonium pectorale is intermediate in size between that of isogamous, unicellular Chlamydomonas reinhardtii and the sex-determining locus of anisogamous, multicellular Volvox carteri:

Hamaji et al. 2016 Table 1

Table 1 from Hamaji et al. 2016. Genome and mating locus properties of Gonium pectorale, Chlamydomonas reinhardtii, and Volvox carteri.

The picture to this point is consistent with the idea that anisogamy requires a larger, more complex mating locus than does isogamy. This picture also has some theoretical appeal: it makes sense that genes encoding differences between the sexes, including differences in gamete size, would be included in the mating locus of an anisogamous species. A general property of mating loci is that they don’t recombine during meiosis, so the male and female versions can diverge. If additional genes, beyond those determining isogamous mating types, are required to encode sex-specific differences in anisogamous species, we should expect that the transition to anisogamy would be accompanied by an increase in the size of mating loci.

By this logic, we would predict that anisogamous Eudorina would have a larger mating locus than isogamous Yamagishiella, Gonium, or Chlamydomonas. Surprisingly, that’s not the case. Hamaji and colleagues’ new paper shows that the mating locus of Eudorina is actually considerably smaller than any of the isogamous species so far characterized:

Hamaji et al. 2018 Fig. 1

Figure 1 from Hamaji et al. 2018. Volvocine green algal phylogeny and mating-type locus (MT) evolution. Phylogenetic relationships of volvocine algae are illustrated with vegetative morphology, gamete morphology, and MT structures of Yamagishiella unicocca, Eudorina sp., and three other species previously studied (Chlamydomonas reinhardtii, Gonium pectorale, and Volvox carteri).

Since female volvocine algae are basically similar to the asexual forms, the evolution of gamete dimorphism (anisogamy) is mainly about the origin of sperm-producing males. The only male-limited gene in Eudorina is the transcription factor MID, which is also limited to the minus mating type in isogamous species (this is how we know that males evolved from the minus mating type). Since additional genes in the sex-determining region are clearly not needed to produce males, Hamaji and colleagues conclude that

…the evolution of males in volvocine algae might have resulted from altered function of the sex-determining protein MID or its target genes.

So we’re still left with two (non-mutually exclusive) possibilities: changes to the MID gene itself may have changed which genes it interacts with (or how it interacts), or there may have been changes in the genes whose expression is controlled by MID. Hamaji and colleagues seem to lean toward the latter possibility:

…in this lineage the transition to anisogamy likely involved direct modification of the sex determination pathway controlled by MID rather than by acquisition of new gamete size control genes in MT.

I suspect they’re right, but we don’t really know at this point. Finding out which genes MID regulates in isogamous and anisogamous species, and what those genes do, would go a long way toward completing the picture.


Stable links:

Hamaji, T., Kawai-Toyooka, H., Uchimura, H., Suzuki, M., Noguchi, H., Minakuchi, Y., et al. 2018. Anisogamy evolved with a reduced sex-determining region in volvocine green algae. Commun. Biol., 1: 17. doi: 10.1038/s42003-018-0019-5

Hamaji, T., Mogi, Y., Ferris, P., Mori, T., Miyagishima, S., Kabeya, Y., Nishimura, Y., Toyoda, A., Noguchi, H., Fujiyama, A., Olson, B., Marriage, T., Nishii, I., Umen, J., Nozaki, H. 2016. Sequence of the Gonium pectorale mating locus reveals a complex and dynamic history of changes in volvocine algal mating haplotypes. G3: Genes|Genomes|Genetics 062386: 1-42. doi: 10.1534/g3.115.026229

Nozaki, H., T. Mori, O. Misumi, and S. Matsunaga. 2006. Males evolved from the dominant isogametic mating type. Current Biology 16:1017–1018. doi: 10.1016/j.cub.2006.11.019

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