Meet Eudorina compacta!

Nozaki et al. 2020 Fig. 2A & B

Fig 2A & B from Nozaki et al. 2020. Light microscopy of Eudorina compacta Nozaki sp. nov. originating from Lake Victoria. (A) Surface view of 32-celled vegetative colony showing compactly arranged cells. (B) Optical section of 32-celled vegetative colony showing a hollow structure.

Hisayoshi Nozaki and colleagues have described another new species of volvocine algae, a member of the genus Eudorina from Lake Victoria in Tanzania. Unlike most species in this genus, the cells of Eudorina compacta are tightly packed around the surface of the colony, which is ellipsoidal. They coexist in Lake Victoria with Colemanosphaera charkowiensis, another species that Dr. Nozaki and colleagues described in 2014.

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Volvox rousseletii in Japan

A few years back, I invited Dr. Hisayoshi Nozaki to visit the University of Montana, and to my surprise, he came. In fact, five Japanese researchers came to Missoula for the better part of a week: Dr. Nozaki, Dr. Noriko Ueki, Dr. Osami Misumi, and two undergraduate researchers. We found a species, Volvox capensis, which had previously only ever been found in South Africa, in Ninepipe Reservoir (about an hour north of Missoula).

Now Ryosuke Kimbara and colleagues have reported another apparent long-distance traveller. In a new paper in PLoS One, they report finding Volvox rousseletii, previously reported only in Africa, in Lake Sagami in Japan. Volvox rousseletii is a member of the group of species known as Volvox section Volvox (also sometimes referred to as Euvolvox), which includes the largest species (in terms of cell number) and evolved independently of the other species in the genus Volvox.

Kimbara Fig. 1

Figure 1 from Kimbara et al. 2019. Light microscopic features of asexual spheroids in culture of Volvox rousseletii strain v-sgm-17 from Lake Sagami, Japan. (A) Mature spheroid showing daughter spheroids (d). (B-D) Part of spheroids. (B) Top view of individual sheaths (asterisks) of somatic cells stained with methylene blue. (C) Top view of somatic cells with thick cytoplasmic bridges (b). (D) Side view of elongate-ellipsoidal, anterior somatic cell with stigma (s) and pyrenoid (p) in the chloroplast. (E) Developing embryo just after inversion, showing gonidia (g) of the next generation.

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Why carteri?

It’s embarrassing, really. I’ve been studying Volvox and its relatives for 15 years now, and until today I couldn’t have told you who the most famous member of the group, Volvox carteri, was named for. Sure, I know Colemanosphaera is named for Annette Coleman, Volvox ferrisii for Patrick Ferris, and Volvox kirkiorum (“of the Kirks”) for David and Marilyn Kirk, but that’s because they were all named after I started studying Volvox.

But do you recall…the most famous algae of all?

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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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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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What is a (Volvox) species?

Hisayoshi Nozaki and colleagues have just described some Volvox samples from two lakes and a pond in Japan.

Figure 1A from Nozaki et al. 2016. Volvox sp. Sagami asexual spheroid with daughter colonies (d).

Figure 1A from Nozaki et al. 2016. Volvox sp. Sagami asexual spheroid with daughter colonies (d).

The newly collected strains have a lot in common with another recently described species, Volvox ferrisii, but there are some important differences as well:

…it could be clearly distinguished from all previously described monoecious species of Volvox sect. Volvox by its small number of eggs or zygotes (5–25) in sexual spheroids, with short acute spines (up to 3 μm long) on the zygote walls and elongated anterior somatic cells in asexual spheroids.

In spite of these differences, Nozaki and colleagues stop short of calling the newly collected strains a new species. Why?

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New Volvox species

Hisayoshi Nozaki and colleagues have done it again: in a new PLoS One article, they have described yet another new species of Volvox, V. reticuliferus (see also “Volvox 2015: taxonomy, phylogeny, & ecology“):

Figure 1A from Nozaki et al. 2015: Surface view of asexual Volvox reticuliferus spheroids.

Figure 1A from Nozaki et al. 2015: Surface view of asexual Volvox reticuliferus spheroids.

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Why don’t we revise volvocine taxonomy?

Volvocine taxonomy is in a sorry state. Most nominal genera, and some nominal species, are almost certainly polyphyletic. More than once, I’ve been asked during a talk, “Why is Volvox scattered all over the tree?”

JPhycol2010Fig2a

Fig. 2A from Herron et al. 2010. The traits characteristic of the genus Volvox—asexual forms with >500 cells, only a few of which are reproductive, and oogamy in sexual reproduction—have arisen at least three times independently: once in the section Volvox (represented by V. globator, V. barberi, and V. rousseletii), once in V. gigas, and once or possibly twice in the remaining Volvox species. Branch shading indicates maximum-parsimony reconstruction (white = absent, black = present, dashed = ambiguous). Pie charts indicate Bayesian posterior probabilities at selected nodes. Numbers to the left of cladograms indicate log-Bayes factors at selected nodes: positive = support for trait presence, negative = support for trait absence. Interpretation of log-Bayes factors is based on Kass and Raftery’s (1995) modification of Jeffreys (1961, Theory of probability. 3rd edn. Oxford Univ. Press, Oxford, UK.): 0 to 2, barely worth mentioning; 2 to 6, positive; 6 to 10, strong; >10, very strong. Boldface numbers following species names indicate Volvox developmental programs following Desnitski (1995).

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