J. S. Huxley part 1: Gonium


Julian Huxley was one of the biologists responsible for the merging of Mendelian genetics and Darwinian evolution in the early 20th century, the modern synthesis. His most influential work was Evolution: The Modern Synthesis, published in 1942. Thirty years earlier, though, he published a book on biological individuality, The Individual in the Animal Kingdom. Thankfully, the copyright on this book has expired, so it is now part of the public domain, and a scanned version is available for free in pdf and epub versions from Google.

Huxley Cover

Any book with Volvox on the cover can’t be all bad!

The Individual in the Animal Kingdom was published around the same time that Huxley accepted a position as the founder of Rice University’s (then Rice Institute’s) biology department. As in previous and subsequent discussions of biological individuality, Volvox and its relatives play a major role:

Illustrating these theoretical points, there exist for us, among various other examples, the members of the family Volvocidae,—an old but well-tried object-lesson. These organisms, claimed by botanist and zoologist alike, are members of the Flagellata, unicellular organisms marked off by possessing long whip-lashes or flagella with which they swim. The Volvocidae seem to be a perfectly natural family. They are all free-swimming; they are all colonial, with a framework of transparent jelly common to the colony; they all possess chlorophyll, nourishing themselves after the fashion of plants; and they all have two flagella, a single “eye-spot” and other morphological characters. There can thus be little doubt that they are all descended from a single ancestor who combined these common characters in his person.

He is almost certainly right about that; although the “Volvocidae” have been revised into three families (Tetrabaenaceae, Goniaceae, and Volvocaceae), nearly all recent phylogenetic studies conclude that they are monophyletic. I love that even in 1912 the volvocine algae were “…an old but well-tried object-lesson.”

At the base of the series stands Gonium—sixteen precisely similar flagellate cells embedded in firm transparent jelly, joined in definite arrangement to form a flat disc (Fig. 7). The colony thus constituted lives and prospers, nourishes itself, and grows till comes the time for reproduction. Then each cell of the sixteen divides—once, twice, thrice, and four times—into sixteen little ones. Each of the sixteen groups of sixteen breaks away from the rest, arranges its parts in the familiar way, and constitutes itself a minute but perfect new colony.

Huxley’s description of autocolony formation is as good as any I’ve heard, and the accompanying figure gives a reasonable visual depiction:

Huxley Figure 7

Fig. 7 from Huxley 1912. Gonium. A, a species containing 16 cells embedded in a flat plate of gelatinous substance. BF, another species, containing 4 cells. B, C, adult colonies, seen from the top and side, respectively. In D one, in E two, and in F all four cells have divided into four. The four groups of four cells in F will shortly separate and become independent daughter-colonies. (Highly magnified.) (From West.)

No “West” is listed in the Lit Cited, but B-F are from Plate III of West & West 1896, where the alga in question was called Tetragonium lacustre (thanks to Erik Hanschen for helping me figure this out). Stein (1959) clarifies that this is Tetrabaena socialis (then classified as Gonium sociale). A is probably Gonium pectorale.

Among all the other members of the family except Volvox, the asexual reproduction (with which alone we need here be concerned) is accomplished in a similar way—each cell takes upon itself to reproduce a whole new colony. They are colonies and nothing more—their members have united together because of certain benefits resulting from mere aggregation, but are not in any way interdependent, so that the wholes are scarcely more than the sum of their parts.

Here I’m afraid Sir Huxley and I part ways. First, and less importantly, not all of the other genera of volvocine algae lack cellular differentiation: Pleodorina and Astrephomene also have somatic and reproductive cells. More importantly, though, I don’t think it’s fair to say that they “are colonies and nothing more” and that their cells “are not in any way interdependent.” All of the members of the family Volvocaceae, which includes Colemanosphaera, Eudorina, Pandorina, Platydorina, Pleodorina, Volvox, Volvulina, and Yamagishiella, undergo complete inversion during development. Stephanie Höhn and Armin Hallmann have published a detailed study of this process in Pleodorina, but the gist is the same for all of the (non-Volvox) genera:

 

Cells within a colony are connected by cytoplasmic bridges at this point in development, and inversion requires a coordinated combination of movements relative to these connections and changes in cell shape:

Figure 11 from Höhn & Hallmann 2016. Model of the inversion process and subsequent development in P. californica. A schematic presentation of inversion as deduced from time-lapse transmitted light microscopy, light microscopy of semi-thin sections and transmitted electron microscopy of thin sections. Mid-sagittal cross-sections of an embryo of P. californica during inversion and subsequent development. Cell content is shown in green; red lines indicate the position of the CB network; nuclei are shown in blue. The directions of the cell layer movements are indicated by black arrows. Frames show the approximate localization of the details presented in Figs. 5, 6, 7, 8, and 9. a Pre-inversion stage. b, c Early inversion stage: the peripheral (anterior) region of the plakea bends outwards. d-f Mid-inversion stage: Bending of the peripheral region of the cell sheet continuous and, simultaneously, the centrally located posterior region of the plakea moves towards the opening of the bowl-shaped cell sheet. g, h Late inversion stage: the entire cell sheet proceeds to bend so that the previously concave plakea becomes more and more convex; at the end of inversion the cell sheet is two-thirds closed. i-k Post-inversion stage: the cells round up and the opening (phialopore) closes; ECM biosynthesis begins. l Young adult shortly after release from its mother spheroid.

Figure 11 from Höhn & Hallmann 2016. Model of the inversion process and subsequent development in P. californica. Cell content is shown in green; red lines indicate the position of the cytoplasmic bridge network; nuclei are shown in blue. The directions of the cell layer movements are indicated by black arrows. a Pre-inversion stage. b, c Early inversion stage: the peripheral (anterior) region of the plakea bends outwards. d-f Mid-inversion stage: Bending of the peripheral region of the cell sheet continuous and, simultaneously, the centrally located posterior region of the plakea moves towards the opening of the bowl-shaped cell sheet. g, h Late inversion stage: the entire cell sheet proceeds to bend so that the previously concave plakea becomes more and more convex; at the end of inversion the cell sheet is two-thirds closed.

I have a hard time thinking about Pleodorina or even Eudorina as anything other than a multicellular organism. Tetrabaena, maybe, but even Tetrabaena cells are connected by cytoplasmic bridges. Aside from inversion, all of the members of the Volvocaceae have an anterior-posterior polarity as defined by the direction of swimming, and their cells are spatially patterned in such a way that all of their flagella beat in the same direction. Of course, whether or not a particular species ‘counts’ as a multicellular organism depends on how we define multicellular organism, and not everyone agrees on where to draw this line. I would argue, though, that even the undifferentiated members of the Volvocaceae are sufficiently integrated to qualify.

Next time, I’ll look at what Huxley had to say about Volvox.

 

Stable links:

Arakaki, Y. et al. 2013. The simplest integrated multicellular organism unveiled. PLoS One 8:e81641.

Höhn, S. & Hallmann, A. 2016. Distinct shape-shifting regimes of bowl-shaped cell sheets – embryonic inversion in the multicellular green alga Pleodorina BMC Dev. Biol. 16:35.

Huxley, J. S. 1912. The Individual in the Animal Kingdom. (Cambridge University Press).

Stein, J. R. 1959. The four-celled species of Gonium. Am. J. Bot. 46:366–371.

West, W. & West, G. S. 1896. On some new and interesting freshwater algae. J. R. Microsc. Soc. 1896:149–165.

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