Pierre Haas on Volvox inversion

Average shapes of Volvox inversion

Figure 4 from Haas et al. 2018. Average shapes of Volvox globator embryos for 10 stages of inversion (red lines), obtained from N = 22 overlaid and scaled embryo halves (lines in shades of blue on the left) and corresponding standard deviation shapes (shaded areas on the right).

One of my search alerts turned up a blog post about Volvox inversion, “Upside Down and Inside Out: Inversion in Volvox.” The author wasn’t identified at the top, but by the third paragraph it was clear that the post was written by someone with a deep familiarity with the subject:

In order to be able to swim, the colony must therefore turn itself inside out through a hole at the top of the cell sheet. This process is called inversion, and proceeds in different ways (type-A and type-B inversion) in different species. (It is not clear why Volvox evolved to have its flagella on the inside after cell division: the closely related alga Astrephomene divides into spherical colonies without the need for inversion.

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Choanoflagellates with inversion

Salpingoeca rosetta

Figure 1A from Dayel et al. 2011. Spherical colony of Salpingoeca rosetta. Scale bar = 5 μm.

The closest (known) living relatives of animals are a group of unicellular or colonial filter-feeders known as choanoflagellates. Much of what we know about the evolution of multicellularity in animals comes from comparisons with choanoflagellates. For example, many of the gene families involved in multicellular development in animals, and previously thought to be unique to animals, have turned out to be present in choanoflagellates as well, suggesting that these gene families were present in animal ancestors before they evolved multicellularity. Some multicellular choanoflagellates have even been shown to have differentiated cell types (Laundon et al. 2019):

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Mary Agard Pocock

Alexey Desnitskiy, Stuart Sym, and Pierre Durand have published a new paper in Transactions of the Royal Society of South Africa recounting the contributions of South African phycologist Mary Agard Pocock to Volvox research [full disclosure: Pierre Durand and I were labmates in Rick Michod’s lab at the University of Arizona for a time, and Alexey Desnitskiy is a friend and collaborator].

Pocock, who defended her Ph.D. in 1932, made careful observations of both sexual and asexual development in several species of Volvox that she collected in southern Africa: V. africanus, V. capensis,V. rousseletii, and V. gigas (which she originally described). For some of these species, hers are still the only detailed descriptions of their ontogeny:

Pocock studied almost all aspects of asexual and sexual development in several African Volvox species, with the exception of sexual differentiation control…Pocock’s data on embryonic inversion in V. africanus, V. capensis, V. gigas and V. rousseletii retain their importance today. Her description of inversion during asexual development in V. africanus and V. capensis remains the only detailed study of this process in these two species and her observations of embryonic inversion in V. gigas and V. rousseletii were corroborated almost 40 years later. [references omitted]

Pocock 1933 Fig. 2L-O

Figure 2L-O from Pocock 1933. Inversion in Volvox gigas.

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This awkward condition

I’ve written several times about the process of inversion that occurs during the development of algae in the family Volvocaceae. Today I was going through a paper I’d read (and even written about) before, and I came across a turn of phrase I appreciated regarding inversion:

The fully cleaved embryo contains all of the cells of both types that will be present in an adult but it is inside out with respect to the adult configuration. This awkward condition is quickly corrected by a gastrulation-like inversion process.

The quote is from Benjamin Klein, Daniel Wibberg, and Armin Hallmann’s 2017 paper, “Whole transcriptome RNA-Seq analysis reveals extensive cell type-specific compartmentalization in Volvox carteri.” Setting aside that animal gastrulation and Volvox inversion may not be as similar as they are often portrayed, I love the description of inside-out colonies as “awkward”. As if they just realized they left the house with their shirt half tucked in and inversion is their way of saying “Excuse me while I get myself sorted out here.”

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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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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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Mechanics of Volvox inversion

Variation is everywhere in biology. Structural variation is present at molecular, cellular, organismal, and population levels, and functional variation occurs in processes from metabolism to development to behavior. In spite of this, we often describe biology in typological terms, and this is often a source of confusion.

Some variation is crucial; for example, evolution is dependent on genetic variation, and behavioral variation within ant and bee colonies ensures that all the necessary jobs get done. Much variation, though, is simply biological noise, an unavoidable consequence of the mostly analogue nature of living systems. In extreme cases, variation of this sort can complicate and even derail development, but in general development is remarkably robust. A variety of regulatory mechanisms prevent small amounts of variation early in development from being amplified into large variations in adults.

Pierre Haas and colleagues have posted a preprint to arXiv describing variation in the developmental process of inversion in Volvox globator. Facultatively sexual organisms such as Volvox are great for studying non-genetic sources of variation, because it’s pretty simple to produce millions of genetically identical individuals. When they are raised in identical conditions, variation due to environmental differences is minimized, and most of the observed variation is stochastic.

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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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