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!

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Pleodorina inversion

Stephanie Höhn and Armin Hallmann have published a detailed study of the developmental process of inversion in Pleodorina californicaPleodorina is one of the two genera we usually refer to as ‘partially differentiated’ (the other is Astrephomene), meaning that some of their cells are specialized for motility and never reproduce (soma) and some perform both motility and reproductive functions. P. californica is pretty big, up to about 1/3 of a millimeter, easily visible to the naked eye (though you’d need better vision than mine to make out any details).

Stephanie Höhn sampling a pond near Cambridge University during the Volvox 2015 meeting.

Stephanie Höhn sampling a pond near Cambridge University during the Volvox 2015 meeting.

Like all members of the family Volvocaceae, P. californica undergoes complete inversion during development:

After the completion of the cell division phase and before inversion, the embryos of Gonium, Pandorina, Eudorina and Pleodorina consist of a bowl-shaped cell sheet, whereas the embryonic cells of Volvox form a spherical cell sheet. With exception of the genus Astrephomene, all multicellular volvocine embryos face the same “problem”: the flagellar ends of all the cells point toward the interior of the bowl-shaped or spherical cell sheet rather than to the exterior, where they need to be later to function during locomotion. [References removed]

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Volvox 2015 meeting review available online

Fig. 1 from Herron 2016. Examples of volvocine species. 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.

Fig. 1 from Herron 2016. Examples of volvocine species. 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. A and B by Deborah Shelton.

The meeting review for the Third International Volvox Conference is now available online at Molecular Ecology (doi: 10.1111/mec.13551). The editors warned me ahead of time that the challenge for this paper would be to make it of broad interest to the readership of Molecular Ecology, so there is a lot of background information that will be old news to members of the Volvox community.

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Volvox 2015: development

Replica of Antonie van Leeuwenhoek's microscope.

Ray Goldstein‘s working (!) replica of Antonie van Leeuwenhoek’s microscope.

At the start of the Development session, I asked for a show of hands of people who self-identify as developmental biologists. About four went up. That’s not quite fair, since there’s some ambiguity in the question (primarily? exclusively?), but my point was that what all of us who are interested in the evolution of multicellularity study is the evolution of development. In fact, it might fairly be said that the origin of multicellularity is the origin of development.

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The most important time in your life

The New York Times has picked up a recent article in Physical Review Letters by Stephanie Höhn and colleagues (Höhn, S., Honerkamp-Smith, A.R., Haas, P. a., Trong, P.K. and Goldstein, R.E. 2015. Dynamics of a Volvox embryo turning itself inside out. Phys. Rev. Lett., 114: 1–5. doi 10.1103/PhysRevLett.114.178101).

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