Are the multicellular volvocine algae monophyletic?

One of the strengths of the volvocine algae as a model system is that they span a range of sizes and degrees of complexity. Sizes range from tens of microns to a couple of millimeters, cell numbers range from one to 50,000 or so, some species do and some don’t have cellular differentiation, and some do and some don’t undergo inversion during development. This variation makes the volvocine algae ripe for comparative analyses, which I and many others have done. It also allows many of the intermediate steps between unicellular and complex multicellular life to be identified, as David Kirk did in his “twelve-step” paper.

The volvocine algae have clearly taken some of those steps more than once. Cellular differentiation, for example, has evolved at least three times, in the genus Astrephomene, in the so-called Volvox section Volvox (a.k.a. Euvolvox), and in the lineage that includes Pleodorina and the other Volvox species. One thing they seem to have only done once, though, is to evolve multicellularity itself.

There have been dozens of studies addressing the evolutionary relationships among various species of volvocine algae. Most have been from Hisayoshi Nozaki’s lab, though I and many others have weighed in as well. Nearly all of them, at least those that address the topic, agree that the three families that make up the multicellular volvocine algae–the Tetrabaenaceae, Goniaceae, and Volvocaceae–uniquely descend from a common ancestor. In other words, the multicellular volvocine algae are monophyletic.

Three important cladistic terms are used to summarize the evolutionary relationships among a group of species. If all of the members of the group descend from a common ancestor, and nothing else descends from that ancestor, the group is called monophyletic. Mammals, for example, are monophyletic. A monophyletic group is also called a clade. If all group members are descended from a common ancestor, but so are some non-group members, the group is called paraphyletic. Reptiles, for example, are paraphyletic, because there is no clade that includes all reptiles that doesn’t also include birds. The word ‘paraphyletic’ should nearly always be followed by ‘with respect to’: reptiles are paraphyletic with respect to birds.

The bottom of the barrel, in terms of evolutionary relationships, is polyphyly. A group is considered polyphyletic if its members don’t share a recent common ancestor at all, in other words, if they have multiple evolutionary origins. Flying animals are polyphyletic. Algae are polyphyletic. The genus Volvox is polyphyletic. Polyphyletic taxa are the scum of the phylogenetic Earth. Telling a taxonomist that a group she has named is polyphyletic is a deadly insult.

The prevailing view of volvocine evolutionary relationships is that the family Volvocaceae is sister to the Goniaceae (that is, each is the other’s closest relative), and the Tetrabaenaceae are sister to the Volvocaceae + Goniaceae. Two new papers infer relationships among volvocine algae and their unicellular relatives, and one of them challenges the view of multicellular monophyly.

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Volvox inversion review

Alexey Desnitskiy from St. Petersburg State University has published a short review of the process of embryonic inversion in the genus Volvox. It is a translation, by the author, of his Russian-language paper in the journal Ontogenez (Desnitskiy, AG. 2018. Ontogenez 49:147-152). The article, in the Russian Journal of Developmental Biology, isn’t listed as open access, but it also doesn’t seem to be paywalled.

Inversion occurs during the development of all known species in the family Volvocaceae (Colemanosphaera, Eudorina, Pandorina, Platydorina, Pleodorina, Volvox, Volvulina, and Yamagishiella), where it serves to turn the embryo inside-out and get the flagella on the outer surface of the colony. The paper discusses the two distinct inversion processes found in different Volvox species:

…the inversion of “type A” and the inversion of “type B,” represented by the two species most thoroughly studied, respectively V. carteri f. nagariensis and V. globator (Hallmann, 2006; Höhn and Hallmann, 2011). The principal difference between these two types of inversion is that this process begins at the anterior pole of the embryo in the first case, while in its posterior hemisphere in the second case. Coordinated displacements of cells relative to the system of intercellular cytoplasmic bridges play, along with changes of the cell shape, an important role in the inversion process in embryos of both Volvox species. In V. globator, though, the spindle-shaped cells could be observed not in the entire embryo but only in the posterior hemisphere at the stage of its compression.

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Multicellularity in Science

I spent the last week of June backpacking in Baxter State Park, Maine. When I finally emerged from the woods, my first stop was Shin Pond Village for a pay shower, a non-rehydrated breakfast, and free internet access. Among the week’s worth of unread emails were a nice surprise and a not-so-nice surprise. The not-so-nice surprise was a manuscript rejected without review; the nice surprise was a new article by Elizabeth Pennisi in Science, which came out when I was somewhere between Upper South Branch Pond and Webster Outlet.

Upper South Branch Pond

Upper South Branch Pond, Baxter State Park, Maine. I spent two nights here.

The article, for which I was interviewed before Baxter, synthesizes recent work across a wide range of organisms that suggests that the evolution of multicellularity may not be as difficult a step as we often assume:

The evolutionary histories of some groups of organisms record repeated transitions from single-celled to multicellular forms, suggesting the hurdles could not have been so high. Genetic comparisons between simple multicellular organisms and their single-celled relatives have revealed that much of the molecular equipment needed for cells to band together and coordinate their activities may have been in place well before multicellularity evolved. And clever experiments have shown that in the test tube, single-celled life can evolve the beginnings of multicellularity in just a few hundred generations—an evolutionary instant.

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Pierre Haas & Stephanie Höhn article on variability in Volvox inversion

Back in September, I reported on an arXiv preprint by Pierre Haas, Stephanie Höhn, and colleagues*, “Mechanics and variability of cell sheet folding in the embryonic inversion of Volvox.” A revised version of that manuscript has now been published in PLoS Biology (“The noisy basis of morphogenesis: Mechanisms and mechanics of cell sheet folding inferred from developmental variability”).

Haas et al. 2018 Fig. 3

Figure 3 from Haas, Höhn, et al. 2018. Inverting Volvox globator embryo visualised by selective plane illumination microscopy of chlorophyll autofluorescence. Top row: maximum-intensity projection of z-stacks. Bottom row: tracing of midsagittal cross-sections; the colour scheme indicates image intensity. Scale bar: 50 μm.

Inversion is a crucial process in the development of algae in the family Volvocaceae (which includes Colemanosphaera, Eudorina, Pandorina, Platydorina, Pleodorina, Volvox, Volvulina, and Yamagishiella), because they start off inside-out, with their flagella pointing inward. Inversion gets the flagella on the outside where they are useful for propulsion.

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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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Nicole Haloupek on germ-soma differentiation

Volvox carteri

Volvox carteri by Gavriel Matt & James Umen.

Back in December, I wrote about two studies that compared global patterns of gene expression between germ cells and somatic cells in Volvox carteri, one by Benjamin Klein, Daniel Wibberg and Armin Hallmann from the University of Bielefeld in Germany and one by Gavriel Matt and Jim Umen from Washington University in St. Louis and the Donald Danforth Plant Science Center, respectively. The Matt & Umen paper has also been highlighted on the Genetics Society of America blog, Genes to Genomes.

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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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That beautiful animalcule: Andrew Pritchard on Volvox

Pritchard figure

Plate from Pritchard 1834. Image from Google Books.

Andrew Pritchard’s 1834 book The Natural History of Animalcules includes several species he classifies as Volvox. Most of them were probably not Volvox, but his Volvox globator certainly was. His description of Volvox begins on page 39. A scanned version is available online at The Biodiversity Heritage Library, but I have used the slightly higher quality scan in Google Books for the plate above.

The animalcules belonging to this genus are of a globular form, and revolve in the water. Some of the species are so large as to be discerned by unassisted vision, while others are very diminutive. Ehrenberg has not demonstrated their digestive organization; but in a note to his table, conceives they ought to follow the monads. In this genus is included that beautiful animalcule, called the Volvox globator, which forms so interesting a spectacle in the Solar and Gas Microscopes.

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Flagellar synchronization in Chlamydomonas

The physics is way beyond me, but a new paper by Gary Klindt and colleagues in New Journal of Physics uses Chlamydomonas as a model for flagellar synchronization:

We present a theory of flagellar synchronization in the green alga Chlamydomonas, using full treatment of flagellar hydrodynamics and measured beat patterns. We find that two recently proposed synchronization mechanisms, flagellar waveform compliance and basal coupling, stabilize anti-phase synchronization if operative in isolation. Their nonlinear superposition, however, can stabilize in-phase synchronization for suitable parameter choices, matching experimental observations.

Klindt et al. Fig. 1

Figure 1 from Klindt et al. 2017. In-phase and anti-phase synchronization. (a) In-phase synchronization at high synchronization strength, corresponding to “breast-stroke swimming” Chlamydomonas. (b) For low synchronization strength, anti-phase synchronization is stable, corresponding to a “free-style” gait.

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