Embryogenesis in Gonium and Tetrabaena

Back when I was a cocky grad student, I wrote a paper that was, in some ways, critical of the work of one of the biggest names in my field. David Kirk, who passed away last year, was among the most important figures in establishing Volvox as a model system for development, genetics, and evolution, among other things. He had published a paper that I thought was unnecessarily progressivist, and I said so in terms that, in retrospect, could have been more diplomatic. In response, Dr. Kirk, whom I had never met, sent me a very thoughtful email thanking me for pointing out some of the problems and politely disagreeing on some other points. Its tone was kind and respectful when annoyed and argumentative would have probably been justified.

In that email, he offered a bet, the stakes of which were to be a beer, that one of the things I had suggested would turn out to be wrong. The issue had to do with inversion, a process that the (mostly) spheroidal algae in the family Volvocaceae undergo during development. I have written about inversion many times on Fierce Roller; in a nutshell, these algae start their lives inside-out, with their flagella on the inside, and invert to get the flagella on the outside, where they can be used for swimming. Their relatives in the genus Gonium also undergo a process of partial inversion, changing from cup-shaped (with the flagella on the concave side) to flat or slightly cup-shaped in the other direction. Dr. Kirk had interpreted Gonium‘s partial inversion as a probable intermediate step that led to the complete inversion characteristic of the Volvocaceae. My reconstructions suggested that incomplete inversion in Gonium had evolved separately from complete inversion in the Volvocaceae, and Dr. Kirk bet me that this would turn out to be wrong.

Figure 3 I&J from Herron & Michod 2008.

Figure 3 I&J from Herron & Michod 2008. Two different ancestral character state reconstructions for inversion, both of which suggest separate origins in Gonium and in the Volvocaceae. Pie charts show the relative likelihoods of alternative states at each node: for I, inversion present (black) or absent (white); in J, complete inversion (black), partial inversion (gray), or no inversion (white). In both cases, the most likely state for the most recent common ancestor of the Volvocaceae and Gonium (red arrows) is no inversion, but the evidence from hypothesis testing is weak (the numbers at the nodes are Bayes factors, where 0 to 2 is barely worth mentioning, 2 to 6 positive, 6 to 10 strong, and >10 very strong).

I’m not quite ready to say this issue is resolved, but a recent paper from the University of Tokyo suggests I may owe Dr. Kirk a beer (sadly, he is no longer around to collect). Shota Yamashita and Hisayoshi Nozaki have studied embryological development in two flattened species of volvocine algae, Gonium pectorale and Tetrabaena socialisGonium is sister to Astrephomene, a spheroidal colony, and together they make up the family Goniaceae, which is in turn sister to the (mostly) spheroidal Volvocaceae. Tetrabaena is one of two known species in the family Tetrabaenaceae, which are sister to the Goniaceae+Volvocaceae:

Yamashita & Nozaki Fig. 1

Figure 1 from Yamashita & Nozaki 2019. Schematic representation of the phylogenetic relationships of volvocine green algae and evolution of their body plans. The evolution of spheroidal colonies is thought to have occurred twice within the volvocine algae, in the ancestors of Astrephomene and in those of Volvocaceae. The formation of spheroidal colonies during embryogenesis is based on different cellular mechanisms in the two lineages. There are two extant lineages with ancestral flattened colonies, the genus Gonium and the family Tetrabaenaceae. All drawings and photographs represent lateral views of individuals with anterior sides (the direction of swimming) oriented toward the top of the figure. [references omitted; see original]

These relationships make Tetrabaena and Gonium crucial for understanding the evolution of volvocine body plans. Yamashita and Nozaki found that, while important differences exist between the processes of partial inversion in Gonium and complete inversion in the Volvocaceae, both involve changes in cell shape, which I interpret as suggesting that such changes were present in the most recent common ancestor of the Goniaceae and Volvocaceae. This is in contrast to the process by which Astrephomene achieves its final configuration, which involves rotation of cells during development. Tetrabaena shows no signs of partial inversion, suggesting that this trait evolved after the divergence of the Tetrabaenaceae from the Goniaceae+Volvocaceae.

The authors conclude,

Our results clearly showed a fundamental difference in the cellular mechanisms of embryogenesis between ancestral flattened colonies, G. pectorale and T. socialis, and spheroidal colonies in the volvocine lineage . Neither G. pectorale nor T. socialis showed the rotation of daughter protoplasts observed during successive cell divisions in Astrephomene. Moreover, though the daughter protoplasts of G. pectorale and T. socialis underwent slight changes in shape, they did not display the formation of acute chloroplast ends after cell division that is seen during inversion in volvocacean species. Considering these developmental characteristics along with the phylogenetic relationships of these volvocine lineages, the most likely scenario for the evolution of these cellular mechanisms in association with the emergence of spheroidal colonies is that the ancestor of Astrephomene developed the rotation of daughter protoplasts after it diverged from the ancestors of Gonium, while the ancestor of Volvocaceae acquired the formation of acute chloroplast ends after it diverged from the ancestors of Goniaceae. [references omitted; see original]


Stable links:

M. D. Herron and R. E. Michod, 2008. “Evolution of complexity in the volvocine algae: Transitions in individuality through Darwin’s eye,” Evolution, 62: 436–451. doi: 10.1111/j.1558-5646.2007.00304.x

S. Yamashita and H. Nozaki, “Embryogenesis of flattened colonies implies the innovation required for the evolution of spheroidal colonies in volvocine green algae,” BMC Evol. Biol., 19: 120. doi: 10.1186/s12862-019-1452-x

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