Spheroids without inversion: Astrephomene development


Algae in the family Volvocaceae are (with one exception) little spheroids that swim around in freshwater lakes, ponds, and puddles. Volvox is by far the most famous of these algae, but there are a number of smaller genera, including Eudorina, Pleodorina, and Pandorina:

Fig. 1 from Herron 2016. Examples of volvocine species. (A) Chlamydomonas reinhardtii, (B) Gonium pectorale, (C) Astrephomene gubernaculiferum, (D) Pan- dorina morum, (E) Volvulina compacta, (F) Platydorina caudata, (G) Yamagishiella unicocca, (H) Colemanosphaera charkowiensis, (I) Eudorina elegans, (J) Pleodorina starrii, (K) Volvox barberi, (L) Volvox ovalis, (M) Volvox gigas, (N) Volvox aureus, (O) Volvox carteri. Figure Credit for A and B: Deborah Shelton.

Fig. 1 from Herron 2016. Examples of volvocine species; D-O are in the family Volvocaceae. (A) Chlamydomonas reinhardtii, (B) Gonium pectorale, (C) Astrephomene gubernaculiferum, (D) Pandorina morum, (E) Volvulina compacta, (F) Platydorina caudata, (G) Yamagishiella unicocca, (H) Colemanosphaera charkowiensis, (I) Eudorina elegans, (J) Pleodorina starrii, (K) Volvox barberi, (L) Volvox ovalis, (M) Volvox gigas, (N) Volvox aureus, (O) Volvox carteri. Figure Credit for A and B: Deborah Shelton.

All of the members of this family have a problem: at the end of cell division, they find themselves in an awkward configuration, with their flagella on the inside. Each cell has two flagella, and the algae need them on the outside to be able to swim. They achieve this through a developmental process called inversion, essentially turning themselves completely inside-out during embryogenesis. Even the one member of the family that is not spheroidal, Platydorina (F in the figure above), undergoes inversion before flattening into a horseshoe shape. The ways in which they do this are complex and diverse (see for example “Pleodorina inversion” and “The most important time of your life“), but not the topic of this post.

The sister group to the Volvocaceae, the Goniaceae, also includes a spheroidal genus, Astrephomene (C in the figure above). Although Astrephomene looks a lot like some of the Volvocaceae, say Eudorina (I) or Pleodorina (J), it doesn’t undergo inversion!

How, then, does Astrephomene end up with its flagella on the outside? Shota Yamashita and colleagues have investigated Astrephomene development to find the answer. In a new article in BMC Evolutionary Biology, researchers from the University of Tokyo and Hosei University report detailed observations of Astrephomene development:

The present study was undertaken to evaluate the cellular or subcellular mechanisms underlying the formation of spheroidal colonies of Astrephomene; to this end, we used light microscopy time-lapse imaging of an actively growing culture of a newly established strain and compared it with that of a volvocacean Eudorina, which has a similar cell number and colony size.

The lead author, Shota Yamashita, presented some of these results at the Third International Volvox Meeting (see “Volvox 2015: development“), but the new paper includes much more detail. Instead of the flashy drama of inversion, Astrephomene moves its flagella to the outside by gradual rotations of the protoplasts (basically the cell minus the cell wall):

Figure 7 from Yamashita et al. 2016. Schematic diagrams of the two mechanisms of spheroidal colony formation in the volvocine algae. In Astrephomene, rotation of daughter protoplasts occurs in conjunction with the movement of basal bodies during successive cell divisions. In Eudorina, protoplast rotation is lacking during successive divisions; a spheroidal colony is formed by means of inversion after successive divisions.

Figure 7 from Yamashita et al. 2016. Schematic diagrams of the two mechanisms of spheroidal colony formation in the volvocine algae. In Astrephomene, rotation of daughter protoplasts occurs in conjunction with the movement of basal bodies during successive cell divisions. In Eudorina, protoplast rotation is lacking during successive divisions; a spheroidal colony is formed by means of inversion after successive divisions.

The paper, which is open access, includes time-lapse movies of several views of Astrephomene development. I’ve embedded just one here; head to the article to see the rest.

Additional file 1 from Yamashita et al. 2016: Time-lapse analysis of anterior-lateral view of embryogenesis in Astrephomene. Note the rotation of daughter protoplasts during successive cell divisions. Scale bar: 5 μm, 900x speed.

As the authors point out, Astrephomene probably represents an independent origin of the spheroidal body plan:

Recent phylogenetic studies of the volvocine lineage have suggested that the spheroidal colony might have evolved from a flattened ancestor in two independent lineages: Volvocaceae and the goniacean Astrephomene.

All members of the Volvocaceae undergo inversion, so inversion was probably present in the most recent common ancestor of the family. Since the other member of the Goniaceae, Gonium, is a flat or slightly curved plate of cells, it seems reasonable that the most recent ancestor of the Goniaceae and Volvocaceae was similar to Gonium, and that Astrephomene and the Volvocaceae evolved spheroidal body plans independently. The lack of inversion in Astrephomene supports this view, since Astrephomene and the Volvocaceae achieve spherical body plans through very different developmental mechanisms. The alternative, a spheroidal ancestor, would require that one lineage or the other switched developmental mechanisms AND that Gonium lost the spheroidal body plan.

Stable links:

Herron M D. 2016. Origins of multicellular complexity: Volvox and the volvocine algae. Mol. Ecol. 25:1213–1223.

Yamashita S, Arakaki Y, Kawai-Toyooka H, Noga A, Hirono M and Nozaki H. 2016. Alternative evolution of a spheroidal colony in volvocine algae: developmental analysis of embryogenesis in Astrephomene (Volvocales, Chlorophyta). BMC Evol. Biol. 16:243.

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