The evolution of undifferentiated multicellularity: the Gonium genome


Blogging took a backseat to the wedding of two dear friends two weekends ago and to morel hunting last weekend, so I’m only now getting around to a post that should have been written weeks ago (I promised on April 22 that it would be out the following week). Last month, Erik Hanschen and colleagues published the Gonium pectorale genome, filling in some crucial bits of the transition to multicellular life in the volvocine algae. This was a big project, taking several years and involving over 20 authors from over a dozen institutions. The final paper is open access in Nature Communications.

I did post an effort to explain some aspects of the paper to the cdesign proponentsists at Evolution News and Views, who, by their own admission, failed to understand it (“After reading this paper, we’re none the wiser.”). I also complained of the science media’s tendency to refer to all algae as ‘pond scum.’ The lead author of the genome paper kindly followed up with a guest post addressing some of ENV‘s other misunderstandings, such as the purpose of model organisms in biology and the difference between ‘assertion’ and ‘evidence’. But now it’s time to dig into what the genome paper actually says.

It starts with a short review of the evolution of multicellularity and the value of the volvocine algae as a model system for understanding this transition (transitions, I should say, because it has happened many times):

…because most multicellular lineages have long diverged from their unicellular relatives, the genomic signature of the transition to multicellularity has been obscured, and consequently this evolutionary process remains enigmatic.

This is an important point. For most multicellular lineages, we have a good idea what their closest living unicellular relatives are: for animals, it is choanoflagellates; for plants, a unicellular green alga called Mesostigma. But animals did not evolve from living choanoflagellates, or plants from Mesostigma, any more than humans evolved from gorillas. We tend to imagine the ancestors of multicellular groups as being similar to their extant (living) unicellular relatives, but that’s not a given. In fact these unicellular species have been evolving just as long since their divergence from their multicellular relatives as the multicellular lineages have.

One of the advantages of the volvocine algae as a model system for understanding the evolution of multicellularity is the relative recency of this transition. I say relative, because it was still a long time ago, around 230 million years by my estimate. This means that the unicellular relatives of Gonium and Volvox have been evolving for a shorter time since they diverged from their multicellular relatives than have choanoflagellates or Mesostigma, and the assumption that Chlamydomonas is similar to the unicellular ancestor of the group is probably not as far off. The other big advantage, in my mind, is that a lot of relatively simple multicellular forms still exist, and these make comparative approaches to understanding the transition fruitful.

Figure 1 from Hanschen et al. 2016. (a) Evolution of cell cycle control (C), expanded ECM (E) and somatic cells (S) are denoted. (b) Micrographs of Chlamydomonas (green; scale bar, 10 μm), Gonium (blue; scale bar, 10 μm) and Volvox (black; scale bar, 25 μm) show morphological differences.

Figure 1 from Hanschen et al. 2016. (a) Evolution of cell cycle control (C), expanded ECM (E) and somatic cells (S) are denoted. (b) Micrographs of Chlamydomonas (green; scale bar, 10 μm), Gonium (blue; scale bar, 10 μm) and Volvox (black; scale bar, 25 μm) show morphological differences.

I’m going to beat this old drum a bit more: restraint is called for in the way we talk about these ‘intermediate’ forms. Chlamydomonas is not an ancestor of Gonium, nor Gonium of Pleodorina, nor Pleodorina of Volvox (if you think Fig. 1 contradicts this, check out this excellent article). We have good reason to think that Volvox had an ancestor not too different from Pleodorina, but we should always bear in mind that this in an inference, not an observation.

At any rate, the existence of intermediate forms (intermediate in terms of size and complexity) has allowed fairly detailed reconstructions of the morphological and developmental changes that led to differentiated multicellularity in Volvox, and a large body of work by David Kirk and various former members of his lab has established the genetics underlying cellular differentiation. However, little was previously known about the genetics underlying the early steps in the evolution of multicellularity. The Gonium genome paper is a big step toward figuring this out.

Consistent with previous work (and despite assertions to the contrary), the evolution of multicellularity, at least in the volvocine algae, appears to involve few new genes. Rather, the genetics underlying this transition appear to result primarily from changes to the sequences or regulation of existing genes:

Notably, we observe that the genetic innovation correlating with multicellularity, shared between Gonium and Volvox, evolved through co-option of existing developmental programs of cell cycle control.

In particular, the simple fact of multicellularity (in the broad sense of just having multiple cells) appears to involve the retinoblastoma gene, which, in humans, acts as a tumor suppressor. The evidence for retinoblastoma’s role in multicellularity in Gonium is compelling: Hanschen and colleagues moved the Gonium version of retinoblastoma to a Chlamydomonas strain that lacked a retinoblastoma gene. When the Gonium gene is expressed in Chlamydomonas, the normally unicellular Chlamydomonas develops multicellular colonies with cell numbers similar to those of Gonium.

Figure 4a from Hanschen et al 2016. Transformation schematic showing resulting morphology overlaid onto cell and colony size measurements (logarithmic scale) of control Chlamydomonas RB mutant (rb or mat3–4, transformed with empty vector), complementing HA-CrRB::rb (two of five independent transformations are shown) and colonial HA-GpRB::rb (four independent transformations are shown). Crossing colonial HA-GpRB::rb to a Chlamydomonas DP1 mutant (dp1) restores unicellularity in Chlamydomonas (one of two independent matings are shown).

Figure 4a from Hanschen et al 2016. Transformation schematic showing resulting morphology overlaid onto cell and colony size measurements (logarithmic scale) of control Chlamydomonas RB mutant (rb or mat3–4, transformed with empty vector), complementing HA-CrRB::rb (two of five independent transformations are shown) and colonial HA-GpRB::rb (four independent transformations are shown). Crossing colonial HA-GpRB::rb to a Chlamydomonas DP1 mutant (dp1) restores unicellularity in Chlamydomonas (one of two independent matings are shown).

Later this week, I’ll post some questions I asked the lead author of the Gonium genome paper, Erik Hanschen (and his answers, of course).

 

Stable links:

Baum DA, Smith SD, Donovan SSS (2005) The tree-thinking challenge. Science, 310, 979–980.

Hanschen ER, Marriage TN, Ferris PJ et al. (2016) The Gonium pectorale genome demostrates co-option of cell cycle regulation during the evolution of multicellularity. Nature Communications, 7, 11370.

Herron MD, Michod RE (2008) Evolution of complexity in the volvocine algae: transitions in individuality through Darwin’s eye. Evolution, 62, 436–451.

Herron MD, Hackett JD, Aylward FO, Michod RE (2009) Triassic origin and early radiation of multicellular volvocine algae. Proceedings of the National Academy of Sciences, USA, 106, 3254–3258.

Kirk DL (2005) A twelve-step program for evolving multicellularity and a division of labor. BioEssays, 27, 299–310.

 

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