Extreme variation in male Volvox carteri from Taiwan

Nozaki et al. 2018 Fig. 1 A-D

Figure 1 a-d from Nozaki et al. 2018. Light microscopy of asexual spheroids in Taiwanese strains of Volvox carteri f. nagariensis. a Surface view of a spheroid showing undivided gonidia (G). 2016‐tw‐nuk‐6‐1. b Optical section of a spheroid in (a) with gonidia (G). c Surface view of spheroid. Note no cytoplasmic bridges between somatic cells. 2016‐tw‐nuk‐6‐1. d Surface view of spheroid showing individual sheaths of the gelatinous matrix. Stained with methylene blue. 2016‐tw‐nuk‐8‐1. e Optical section of gonidium. 2016‐tw‐nuk‐6‐1. f, g Pre‐inversion plakea or embryo (E) showing gonidia (G) of the next generation outside. 2016‐tw‐nuk‐8‐1.

Most of what we know about the developmental genetics of Volvox comes from the Eve strain of Volvox carteri forma nagariensis, which was collected by Richard Starr from Kobe, Japan in 1967. Eve is the strain that David Kirk and colleagues used for most of their experiments and from which most of the important developmental mutants are derived.

It’s natural, then, to think that Eve is representative of V. carteri f. nagariensis and that what’s true for Eve is generally true for this forma. Recent work from Hisayoshi Nozaki and colleagues shows that, at least in one respect, this is a bad approximation.

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Origins of the sexes: more on MID

Last week, I wrote about Takashi Hamaji’s new paper characterizing the mating-type/sex-determining loci in Eudorina and Yamagishiella. That paper showed that the sex-determining region of anisogamous Eudorina is, surprisingly, considerably smaller than the mating-type loci of isogamous Chlamydomonas, Gonium, or Yamagishiella. Because only one gene, MID, is present in the male version of the sex-determining region in Eudorina, Hamaji and colleagues concluded that

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

I commented that

…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.

Now Sa Geng and colleagues have provided at least a partial answer. In a new paper in Development, they swapped versions of MID among different volvocine species* (unfortunately, no unpaywalled version of the paper is currently available; I will add a link when I find one). We already knew that MID is necessary and sufficient for male development: genetically male Volvox carteri colonies that have MID expression turned off produce eggs, and genetically female colonies transformed with MID produce sperm packets (“Sex change (in Volvox)”). But that’s MID from the same species. It’s somewhat surprising that a single gene can cause Volvox to switch sexes, but at least Volvox MID evolved side-by-side with the genes whose expression it controls.

What would be really surprising is if MID from other species, species that diverged from the Volvox lineage ~200 million years ago, worked in Volvox. It would be extraordinarily surprising if MID from a species that doesn’t even have males  could control their development in Volvox. It won’t work. Waste of time; don’t bother trying.

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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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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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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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New review of green algal sex

Hiroyuki Sekimoto from Japan Women’s University has published a review of sexual reproduction in the volvocine algae and in the Charophyte Closterium in the Journal of Plant Research. In addition to a brief description of the Chlamydomonas sexual cycle, it includes a succinct review of the genetics of sex and sex determination. Unfortunately, the article is paywalled, and my inquiry to the author has so far gone unanswered.

Figure 1 from Sekimoto 2017. The life cycle of Chlamydomonas reinhardtii. Vegetative cells (V) di erentiate into mt+ and mt− gametes (G) during nitrogen starvation (−N). Mating types are restricted by mating-type loci (+ and −). When gametes are mixed, the plus and minus agglutinin mol- ecules on their agellar surfaces adhere to each other, and this adhe- sion results in increased intracellular cAMP levels. The signal trig- gers gamete cell wall release and mating-structure activation. Cells then fuse to form binucleate quadri agellated cells. Zygotes with thick cell walls germinate in response to light and nitrogen supple- mentation, and undergo meiosis to release four haploid vegetative cells

Figure 1 from Sekimoto 2017. The life cycle of Chlamydomonas reinhardtii. Vegetative cells (V) differentiate into mt+ and mt− gametes (G) during nitrogen starvation (−N). Mating types are restricted by mating-type loci (+ and −). When gametes are mixed, the plus and minus agglutinin molecules on their flagellar surfaces adhere to each other, and this adhesion results in increased intracellular cAMP levels. The signal triggers gamete cell wall release and mating-structure activation. Cells then fuse to form binucleate quadriflagellated cells. Zygotes with thick cell walls germinate in response to light and nitrogen supplementation, and undergo meiosis to release four haploid vegetative cells.

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Algae porn

I track the #Volvox hashtag on Twitter, which is how I find out about a lot of the off-label uses of the name Volvox, like DJ Volvox, Volvox the ship, and Volvox the art gallery. Every now and then, it even turns up something related to Volvox the little rolling algae. The other day, @QuintaSwinger tweeted the following video with #Volvox:

The Twitter handle is about just what you think it is; apparently volvocine sex puts someone in mind of polyamory. I suppose I can see that: when a sperm packet enters a colony, it gets busy with all the ova. The video was uploaded to YouTube by Dr. Donald Ott from the University of Akron.

I think the algae in the video are not actually Volvox, though. Certainly the still photo at the beginning is Volvox. Probably not section Volvox (too few cells), and probably not Developmental Program 2 (germ cells too small in the one on the lower right). If I had to guess, I’d say V. aureus, but that’s largely a Bayesian bet because they’re so common. Maybe Alexey Desnitskiy or Hisayoshi Nozaki can comment.

The colonies in the video, though, look more like Pleodorina to me. Not P. sphaerica, since the somatic cells are all in the front, but without more information I can’t narrow it down more than that.

Sex change (in Volvox)

Alexey Desnitskiy from Saint Petersburg State University has published a new review of sexual development in the genus Volvox in the International Journal of Plant Reproductive Biology. 

The article includes an up-to-date review of Professor Desnitskiy’s own work describing four developmental “programs” in the various species of Volvox:

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Origins of the sexes: isogamy and anisogamy

Sex didn’t always involve males and females. I know it still isn’t always between males and females, but that’s not what I mean. I mean that there was a time when sex was happening, but there were no males and females. Sex existed before males and females, and many species are still doing it without them.

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Origins of the sexes: Takashi Hamaji on mating type determination

The evolution of sex is one of the big outstanding problems in evolutionary biology. The origin of sex is one of Maynard Smith and Szathmáry’s “Major Transitions,” on which I’m currently teaching a course here at the University of Montana. Our discussion of sex luckily coincided with the visit of the grad-invited Distinguished Speaker, Sally Otto, an important theorist on this topic (among others). Dr. Otto generously agreed to join us for the discussion, which turned out to be one of the best we’ve had.

A related problem to the origin of sex is the origin of males and females. Sexual reproduction doesn’t always involve males and females: lots of species that don’t even have males and females have sex. There are lots of traits that we associate with males and females — fancy plumage, differences in body size and type of genitalia, presence and absence of exaggerated weapons — but what actually defines males and females is differences in gamete size. Animals, plants, and other organisms with males and females are oogamous: males have small, swimming sperm, and females have large, immotile eggs. But lots of single-celled eukaryotes have only one size of gamete. We call these isogamous (‘equal gametes’).

Some volvocine algae are isogamous (such as Chlamydomonas), some are oogamous (such as Volvox), and some (such as Pleodorina) are anisogamous (‘unequal gametes’), meaning that the gametes come in two sizes but both can swim. In spite of not having sexes per se, Chlamydomonas, like a lot of isogamous organisms, comes in two ‘mating types’, which are arbitrarily called ‘plus’ and ‘minus.’ The mating types are self-incompatible, in other words plus can only mate with minus and vice versa.

All this variation in mating systems makes the volvocine algae a great model system for understanding the evolution of sex and the sexes (see ‘Volvox 2015: all about sex‘). We know from previous work that males evolved from the minus mating type and females from the plus in this lineage. But males and females have evolved from isogamous ancestors many times, and to my knowledge we don’t know which came from which for any other group.

Takashi Hamaji and colleagues have just published an analysis of the genomic region that determines mating type in Gonium pectorale, an isogamous alga more closely related to Volvox than to Chlamydomonas.

Figure 1 from Hamaji et al 2016. A schematic diagram for phylogenetic relationships of selected volvocine species based on Nozaki et al. (2000); Herron and Michod (2008). The top row illustrates gamete type and structure. Tubular mating structures in isogamous gametes are indicated with red bars at the flagellar base. The possession of a MID gene is shown next to the minus mating type or male gametes. The lower row of cartoons depicts vegetative morphology (not to scale) for the indicated species.

Figure 1 from Hamaji et al 2016. A schematic diagram for phylogenetic relationships of selected volvocine species based on Nozaki et al. (2000); Herron and Michod (2008). The top row illustrates gamete type and structure. Tubular mating structures in isogamous gametes are indicated with red bars at the flagellar base. The possession of a MID gene is shown next to the minus mating type or male gametes. The lower row of cartoons depicts vegetative morphology (not to scale) for the indicated species.

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