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.

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Clues to the evolution of multicellularity from Tetrabaena

One development I’m excited to see among the Volvox community is an increased focus on Tetrabaena, one of the smallest and simplest of the colonial volvocine algae. The one species in this genus, Tetrabaena socialis, was classified as Gonium until 1994, when Hisayoshi Nozaki and Motomi Itoh revised it not only to a new genus but a new family, the Tetrabaenaceae.

Nozaki & Itoh 1994 Fig. 10

Figure 10 from Nozaki & Itoh 1994. Summary of the phylogenetic relationships within the colonial Volvocales inferred from cladistic analysis based on morphological data.

Their classification was based on morphological characters, but the backbone relationships, Tetrabaenaceae sister to Goniaceae + Volvocaceae, have subsequently been supported in several independent analyses using genetic data.

In 2013, very much to my surprise, Yoko Arakaki and colleagues showed that the (typically) four cells of Tetrabaena are connected by cytoplasmic bridges (this means that some of the ancestral character state reconstructions I did in grad school need to be revised). Their detailed analyses of Tetrabaena morphology and development are a valuable resource for comparative studies.

Now, in addition to the morphological data, we also have complete sequences for both organelle genomes (mitochondria and chloroplast) and for the nuclear genome. Jonathan Featherston and colleagues published the organelle genomes in 2016, and their new paper in Molecular Biology and Evolution describes the nuclear genome.

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Volvox 2017: Vexed Volvocines

Zach Grochau-Wright

Zach Grochau-Wright

Zach Grochau-Wright has kindly given me permission to print the haiku he presented at the Volvox 2017 meeting in St. Louis. Zach may be the most prolific artist in the obscure sub-genre of volvocine poetry, having previously written and performed “Volvocine rap” at the Volvox 2015 meeting. Here it is in its barely-longer-than-his-name entirety:

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Evolution of outcrossing and selfing

Sex is costly. You could die trying to find a mate. Your mate could kill you, or give you a disease. You could be unable to find a mate in the first place, in which case you’d be better off if you could reproduce asexually. Even without those risks, though, even in a simple genetic simulation, sexual reproduction means you only pass on half of your genes to your offspring.

So why do it? We know that it’s possible to reproduce without sex; lots of things do. It’s not just bacteria and protists, either: asexual reproduction occurs in some plants, insects, snails, amphibians, and reptiles, among many others. The logic of natural selection suggests that sex must confer some benefit that outweighs all the costs, at least in some situations. Essentially all of the proposed benefits of sex have to do with outcrossing, or mixing your genes with those of another, genetically distinct, individual.

Nevertheless, a lot of things that reproduce sexually do so without outcrossing. This is especially common in plants, where it’s called “self-pollination” or just “selfing.” Selfing is thought to provide short-term advantages relative to outcrossing–basically by avoiding the costs I’ve listed above. However, selfing also doesn’t provide most of the benefits associated with sex, so it’s thought to be a bad strategy in the long term. This leads to selfing being thought of as a “dead-end” strategy: the short-term advantages make it unlikely that a selfing species will return to outcrossing, and the reduced genetic variation produced by selfing make diversification less likely.

Erik Hanschen and colleagues have tested these predictions in the volvocine algae (I’m among the “colleagues,” as are John Wiens, Hisayoshi Nozaki, and Rick Michod): do selfing species ever return to outcrossing, and do they have a lower rate of diversification than outcrossing species? Both mating systems exist within the volvocine algae, and so they make a good test case. Roughly speaking, the term heterothallic refers to outcrossing species and homothallic to selfing species:

Hanschen et al. Fig. 1

Figure 1 from Hanschen et al. 2017. Diversity of mating systems in the volvocine green algae and their respective life cycles. (A) In outcrossing (heterothallic) species, distinct genotypes (male on left and female on right) sexually differentiate producing either eggs or sperm. A diploid zygospore (red) is produced after fertilization. Sexual offspring hatch and enter the haploid, asexual phase of the life cycle. (B) In selfing (homothallic) monoecious species, a single genotype is capable of producing both gamete types. Upon sexual differentiation, each sexual colony produces both sperm and eggs. (C) In selfing (homothallic) dioecious species, a single genotype sexually differentiates, producing either eggs or sperm, but not both within the same colony. Cartoons in panels (A–C) are shown with anisogamous, Volvox-like morphology for illustrative purposes only.

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A cautionary tale on reading phylogenetic trees

I have written before about the perils of naive interpretations of phylogenetic trees (“Extant taxa cannot be basal“). Others, notably Krell & Cranston and Crisp & Cook, have pointed out that this is not just a language issue; such misreadings can cause substantive problems in the way evolutionary history is understood.

A new paper in PLoS ONE, “A tree of life based on ninety-eight expressed genes conserved across diverse eukaryotic species,” contains several instructive examples. PLoS ONE is open access, so you can read the original paper without an institutional subscription. A tweet by Frederik Leliaert got this paper on my radar, and it piqued my interest because of the startling observation that the inferred phylogeny shows Chlamydomonas as sister to all other eukaryotes.

It made me frown, too.

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Mechanics of Volvox inversion

Variation is everywhere in biology. Structural variation is present at molecular, cellular, organismal, and population levels, and functional variation occurs in processes from metabolism to development to behavior. In spite of this, we often describe biology in typological terms, and this is often a source of confusion.

Some variation is crucial; for example, evolution is dependent on genetic variation, and behavioral variation within ant and bee colonies ensures that all the necessary jobs get done. Much variation, though, is simply biological noise, an unavoidable consequence of the mostly analogue nature of living systems. In extreme cases, variation of this sort can complicate and even derail development, but in general development is remarkably robust. A variety of regulatory mechanisms prevent small amounts of variation early in development from being amplified into large variations in adults.

Pierre Haas and colleagues have posted a preprint to arXiv describing variation in the developmental process of inversion in Volvox globator. Facultatively sexual organisms such as Volvox are great for studying non-genetic sources of variation, because it’s pretty simple to produce millions of genetically identical individuals. When they are raised in identical conditions, variation due to environmental differences is minimized, and most of the observed variation is stochastic.

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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.

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A confused mess, part 1

I follow Uncommon Descent to keep up with what the cdesign proponentsists are up to, even though I’ve been banned from commentingUncommon Descent pushes out about three times as many articles as Evolution News & Views, and it’s clear that less than a third as much thought goes into each one. Worse, the articles’ authorship is rarely identified, robbing me of my second favorite sport after fly fishing, pointing out creationists’ self-contradictions. For both of these reasons, I don’t comment on their posts nearly as often. But if you read this blog at all, you must know that I can’t pass on a video that 1) claims to provide evidence against evolution and 2) has Volvox in it.

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