Another step toward understanding sex determination in Volvox

Volvox and its relatives are a great model system for understanding the evolution of multicellularity. Their simplicity (relative to most other multicellular groups) and the variety of ‘intermediate’ species (‘intermediate’ in terms of size and complexity) make them especially suitable for comparative studies of their morphology, development, genetics, genomics, and so on. David Kirk’s book on the topic thoroughly reviews the work done up through the late ’90s, and advances since then have only increased the pace of discovery.

But in the last ten years or so, I would argue that the volvocine algae have emerged as a leading model system for an entirely different set of questions related to the evolution of the sexes. Males and females are defined by the gametes they produce, and the sexes came into existence when their gametes diverged into two different types. The existence of different male and female gametes (sperm and eggs, in most cases) is called anisogamy, and the ancestral condition of similar gametes is isogamy.

In 2006, Hisayoshi Nozaki and colleagues reported that volvocine males evolved from the minus (isogamous) mating type. To the best of my knowledge, this is the only group for which we know this. Since then, more clues have been forthcoming, and these were competently reviewed last year by Takashi Hamaji and colleagues. A new paper in PLoS ONE, by Kayoko Yamamoto and colleagues, adds another piece to the puzzle.

Figure S2 from Yamamoto et al. 2017. Light microscopic images of Volvox africanus (homothallic, monoecious with males type) and V. reticuliferus (heterothallic, dioecious type). Scale bars = 50 μm. sp: sperm packet, e: egg. A-C. V. africanus strain 2013-0703-VO4. A. Asexual spheroid. B. Monoecious spheroid. C. Male spheroid. D, E. V. reticuliferus. D. Male spheroid in male strain VO123-F1-7. E. Female spheroid in female strain VO123-F1-6.

Yamamoto and colleagues took advantage of a unique situation to explore the genetic basis of maleness in two species of Volvox. The first advantage to the species they chose is that, although they are very closely related, one (Volvox reticuliferus) is heterothallic and the other (Volvox africanus) is homothallic. In essence, what that means is that Volvox reticuliferus has genetic sex determination and Volvox africanus doesn’t. Since Volvox mostly reproduces asexually, we can isolate one colony and let it reproduce to generate a test tube full of genetically identical colonies. In Volvox reticuliferus, the colonies in that test tube will either be genetically male or genetically female, that is, when they enter the sexual cycle, they’ll all produce either sperm or eggs; never both. If you want to mate Volvox reticuliferus, you need to mix two test tubes, one genetically male and one genetically female. Not so for Volvox africanus. A test tube full of Volvox africanus, even if they’re all genetically identical, can produce both sperm and eggs.

The second feature that Yamamoto and colleagues took advantage of, and this is the really genius bit, is that Volvox africanus that have entered the sexual cycle include both male colonies, which produce only sperm, and hermaphroditic, or monoecious, colonies, which produce both sperm and eggs. This makes possible direct comparisons between male and hermaphroditic colonies that are genetically identical.


Yamamoto Fig. 1

Figure 1 from Yamamoto et al. 2017. Life cycle diagrams for two related species of Volvox.
(A) V. reticuliferus (heterothallic, dioecious type). Germination of a diploid zygote yields a single meiotic product: either a female or a male depending on which mating type locus is inherited. The algae reproduce asexually and can undergo sexual induction to produce sperm packets (in male lineages) or eggs (in female lineages). (B) V. africanus (homothallic, monoecious with males type). Germination of a diploid zygote yields a single meiotic product that reproduces asexually. Upon sexual induction, a clonal population can produce both spheroids containing sperm packets only (male spheroids) and spheroids containing both eggs and sperm packets (monoecious spheroids).

Yamamoto and colleagues compared expression levels of the MID gene in sexual and asexual colonies of Volvox reticuliferus, Volvox africanus, and a more distantly related species, Volvox ferrisii. MID is known to be involved in determining maleness in other volvocine species.

Figure 5D-F from Yamamoto et al. 2017. Semi-quantitative RT-PCR of MID orthologs in three species of Volvox. Gel band quantification analyses by ImageJ. Bars show means and standard deviations of three individual experiments.

The comparisons showed that MID is overexpressed in male colonies of both Volvox africanus and Volvox reticuliferus (and in the hermaphroditic/monoecious colonies of Volvox ferrisii) compared to asexual colonies. However, MID is underexpressed in hermaphroditic/monoecious colonies of Volvox africanus. MID clearly plays a role in sex determination, even in the homothallic Volvox africanus, but it can’t be the whole story, since it is also highly expressed in monoecious colonies of Volvox ferrisii. MID may be necessary for the production of sperm, but its expression (alone) does not prevent the production of eggs.

Since the MID gene is present only in males in species with genetic sex determination, the authors suggest that homothallic species may descend from male genotypes:

…the homothallic species V. africanus might have evolved directly from a male strain of the heterothallic ancestor by modification of the regulation system of MID expressions in sexual spheroids.

This is a fascinating possibility. I’ll even indulge in some speculation that would probably never make it through peer review. The most recent common ancestor of Volvox reticuliferus and Volvox africanus most likely had genetic sex determination. After the two lineages diverged, the ancestors of Volvox africanus could have lost its females, possibly through some extreme population bottleneck. This could, for example, happen through a rare long-distance dispersal event in which a genetically male strain became geographically isolated from the ancestral population. Through asexual reproduction, the male strain could have become numerous if conditions were suitable. If a mutation arose in this (now large) population that caused the formation of hermaphroditic colonies, the mutation would have a massive fitness advantage the next time the population became sexual. That advantage would decrease as the mutation became more common, but it could still, through selection or drift, take over the population, which would at that point be completely homothallic.

This is nothing but a plausible scenario; I don’t have evidence to support any of it. I will note, though, that reducing MID expression in Volvox carteri males is sufficient to produce hermaphroditic colonies. If that was also true for the ancestors of Volvox africanus, a mutation that simply reduced MID expression would do the trick.


Stable links:

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

Yamamoto, K., H. Kawai-toyooka, T. Hamaji, Y. Tsuchikane, T. Mori, F. Takahashi, H. Sekimoto, P. J. Ferris, and H. Nozaki. 2017. Molecular evolutionary analysis of a gender-limited MID ortholog from the homothallic species Volvox africanus with male and monoecious spheroids. PLoS ONE 12:e0180313. doi: 10.1371/journal.pone.0180313

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