Multicellularity rundown


Too many papers, not enough time: each of these deserves a deep dive, but my list just keeps getting longer, so I’m going to have to settle for a quick survey instead. To give you an idea of what I’m up against, these papers were all published (or posted to bioRxiv) in July and August, 2016. By the time I could possibly write full-length posts about them all, there would probably be ten more!

First, a couple of post-Gonium-genome review papers on volvocine algae. In Developmental Biology, Gavriel Matt and James Umen review Volvox development and argue that Volvox “…is an excellent model for the investigation of developmental mechanisms and their evolutionary origins.”

The Volvox body plan is patterned through a stereotyped developmental program that is characterized by processes similar to those found in animals and land plants such as embryogenesis from a single cell, tissue remodeling, and spatially controlled cell type specification. Volvox is a well-developed model organism that is easy to culture, has relatively few cells and cell types, and possesses fast generation times. A growing arsenal of genetic and molecular genetic tools has also been developed for Volvox, including a reference genome sequence, nuclear transformation and expression of transgenes, forward genetics through crosses and transposon-tagging, and reverse genetics through RNAi-mediated or antisense knockdown. [references omitted]

The paper focuses on three developmental processes that are likely to be of interest to developmental biologists outside of the Volvox community: embryogenesis, inversion, and germ-soma differentiation. It brings Kirk’s classic 12-step framework up to date with more recent work and presents a detailed review of the developmental genetics underlying some of the steps. Finally, Matt and Umen pose some “Key questions for future studies:”

What are the mechanisms for establishing and interpreting embryonic polarity?

How does cell size determine cell fate?

What are the differences between germ and somatic cells and what are the regulators that control differentiation?

What are the origins of developmental innovations in Volvox and other volvocine algae?

In Current Opinion in Genetics & Development, Bradley Olson and Aurora Nedelcu review the roles of co-option of existing genes and pathways in the evolution of volvocine multicellularity (full disclosure: Aurora is a close friend and collaborator).

Figure 1 from Olson & Nedelcu 2016. Evolution of multicellular and developmental complexity in the Volvocales. Representative volvocine species with distinct levels of complexity, from single-celled individuals (Chlamydomonas) to complex multicellular organisms with two specialized cell types (Volvox). Genes that have been co-opted for novel morphological and developmental traits in this group have been mapped according to the current understanding of their evolutionary history.

Figure 1 from Olson & Nedelcu 2016. Evolution of multicellular and developmental complexity in the Volvocales. Representative volvocine species with distinct levels of complexity, from single-celled individuals (Chlamydomonas) to complex multicellular organisms with two specialized cell types (Volvox). Genes that have been co-opted for novel morphological and developmental traits in this group have been mapped according to the current understanding of their evolutionary history. Bummer that “Pleodorina star” made it through proofreading (it should be “starrii“).

The examples they give are the co-option of the retinoblastoma protein for simple multicellular development; of regA for germ-soma differentiation; and of genes underlying inversion, asymmetric division, and production of extracellular matrix:

First, the cell cycle was reprogrammed via co-option of RB and cyclin D1 genes to promote the evolution of undifferentiated multicellularity by modifications to the multiple fission division pattern as observed in the extant Gonium. Interestingly, the ancestral multiple fission type of division has been further modified in distinct Volvox lineages, contributing to the four developmental programs known in this group. In the lineage leading to V. carteri, a series of additional co-option events took place, including co-option of genes involved in the structure and function of ECM, embryonic inversion, asymmetric cell division, and establishing the somatic cell fate. Of particular interest is the co-option of regA in the differentiation of soma. Because soma evolved independently in several volvocine lineages, including species whose developmental programs do not involve asymmetric divisions and multiple fission, further sequencing of volvocalean genomes and genetic analyses should reveal whether somatic cell evolution involved similar or distinct genetic mechanisms in this group. [references omitted]

In Development Genes and EvolutionAlexey Desnitskiy analyzes the biogeography of the nominal genus Volvox. Nominal, because Volvox is almost certainly polyphyletic, with three or perhaps four independent origins of the morphological traits that have caused these distantly related species to be classified together. Full disclosure here, too: Alexey and I are friends and colleagues. He suggests that three independent transitions from rapid, palintomic (multiple fission) cell divisions to slow, light-dependent divisions may have been adaptations to short winter days in high latitudes during warm climates 30-60 million years ago. The ecological conclusions are necessarily tentative, but the article serves as a nice summary of what we know about the biogeography of Volvox.

In non-volvocine multicellularity news, Mary Wahl and Andrew Murray tested hypotheses about germ-soma differentiation using engineered yeast strains. They genetically modified Saccharomyces cerevisiae to produce slow-growing ‘somatic’ cells, multicellular clusters, or both. The somatic cells secrete the enzyme invertase, which breaks down sucrose, which yeast can’t eat, into glucose and fructose, which they can. Somatic cells, in this system, are permanently differentiated: they arise sporadically from reproductive cells, but they can only produce more somatic cells.

The authors then competed the engineered, soma-producing strains against non soma producing yeast of the same cellularity, i.e. unicellular invertase secretors versus unicellular non-secretors and multicellular secretors versus multicellular non-secretors. In the unicellular competition, the undifferentiated strains outcompeted the differentiated ones and took over the population. In the multicellular case, though, the soma-producing strains consistently outcompeted the undifferentiated strains.

The somatic cells in this experiment provide an advantage to the cells around them: the invertase they secrete breaks down an inedible sugar into two edible ones. The problem with a public good like invertase, though, is that once you secrete it into liquid medium, anyone can use it. In a well-mixed culture, that means that members of your own strain are no more likely to benefit than members of a competing strain, which is not paying the cost of producing slow-growing invertase secretors. The undifferentiated strain thus grows faster and takes over the population. However, in the multicellular competition experiment, the somatic cells are physically attached to their non-secretor relatives, which therefore gain a disproportionate share of the glucose and fructose. When sucrose is the only food source available, this benefit outweighs the cost of producing somatic cells, and the differentiated strain takes over the population.

Wahl and Murray conclude that, because differentiated unicells are vulnerable to invasion by undifferentiated competitors, differentiated unicellularity is unlikely to have led to differentiated multicellularity. More likely, the first step toward differentiated multicellularity was undifferentiated multicellularity, followed by the evolution of somatic differentiation. This is consistent with the observation that there are lots of undifferentiated multicellular organisms but few differentiated unicellular ones (The authors say there are no examples of unicells with soma, but I’m not sure this is exactly right. For example, lysing Salmonella cells might be considered soma, as might some of the numerous examples of programmed cell death in unicells).

Finally, María Rebolleda-Gómez and colleagues posted a paper to bioRxiv, “Evolution of simple multicellularity increases environmental complexity”. Full disclosure: some of the coauthors are my collaborators, and I’ve written about the yeast experimental system before (check out this video to see Will Ratcliff introducing himself).

In the new paper, Rebolleda-Gómez et al. found that yeast populations under selection for increased settling rate not only evolve simple multicellularity within weeks, they also diversify into two distinct multicellular life histories:

Figure 1 from Rebolleda-Gomez et al. 2016. Diversity on size distributions of isolates from one of the replicate populations. (A) Volume (weighted by total biomass) of different multicellular isolates throughout the duration of the selection ex- periment. Each value is the average of three replicates, each composed of six different fields of view and at least 70 individuals. Big and Small groups can be recognized statistically based on a Tuckey HSD test with significance level of 0.01. Error bars are 95% confidence intervals. (B, C) Pictures showing typical adult and propagule size of the two main strategies described:Big (red) and small (blue).

Figure 1 from Rebolleda-Gómez et al. 2016. Diversity on size distributions of isolates from one of the replicate populations. (A) Volume (weighted by total biomass) of different multicellular isolates throughout the duration of the selection experiment. Big and Small groups can be recognized statistically based on a Tuckey HSD test with significance level of 0.01. Error bars are 95% confidence intervals. (B, C) Pictures showing typical adult and propagule size of the two main strategies described: Big (red) and small (blue).

Reciprocal invasion experiments show that the coexistence of big and small clusters is stable and negative frequency dependent. Cluster size does trade off with growth rate, but simulations show that this is not enough to explain stable coexistence. Rather, coexistence involves hydrodynamic interactions between clusters of different sizes that give the rare type, whichever it is, a selective advantage. Essentially, when small colonies are common, large colonies succeed by settling faster. When large colonies are common, though, they interfere with each other’s settling, allowing smaller colonies to slip between them and get to the bottom faster.

An interesting finding: yeast under settling selection don’t just evolve simple multicellularity, they diversify. In retrospect, maybe we shouldn’t be terribly surprised. Over and over again in microbial evolution experiments, we find that even the most homogeneous environments lead to stable coexistence of two or more strains (for example in the Long-Term Evolution Experiment). Of course, it’s easy to say we shouldn’t be surprised after the fact; I’m not aware of anyone predicting this would happen before the fact (I certainly didn’t).

Not surprisingly, as with pretty much every experimental result related to the evolution of multicellularity, the Discovery Institute is compelled to mock it (without providing arguments or evidence that it’s wrong). This time, it’s David Klinghoffer at Evolution News and Views (“Cambrian Explosion Explained by Yeast Clumping Together“). As is so often the case, he’s reacting not to the research article itself but to a news article about the research article (“Simple lab life makes an evolutionary leap in a few generations“). Like most of the cdesign proponentsists, he’s committed to the delusion that the Cambrian explosion represents an insurmountable challenge to evolutionary theory, and Bob Holmes, the author of the New Scientist article, was so bold as to draw a parallel between diversification in the lab and in nature:

This provides experimental proof that when evolution makes a great leap forward – such as the origin of multicellularity — organisms can diversify rapidly to take advantage of the change.

Many years ago, palaeontologist Stephen Jay Gould suggested that a similar sudden ecological diversification may have led to the Cambrian Explosion in which most animal body forms arose in the fossil record within a few tens of millions of years.

“Possibly what we see here is the first step of what Gould’s talking about – the opening up of diversity due to a key innovation,” says Travisano.

Klinghoffer straw-mans (can I use that as a verb?) this as

Yeast cells clump together. Ergo trilobites.

“Possibly,” given a “few tens of millions of years,” this could represent a “first step” toward massive diversification.

Sounds reasonable to me. He makes it sound as if Holmes is dancing around some greater point…that is the point.

Ann Gauger has written here about not entirely dissimilar speculations about the development of multicellularity, with Volvox rather than yeast as the illustration. “Saying that something might have happened,” she observes, “is not the same as showing that it actually could happen.”

No, showing that it actually could happen, as Rebolleda-Gómez and colleagues have done, is the same as showing that it actually could happen.

 

Stable links:

Ackermann, M., B. Stecher, N. E. Freed, P. Songhet, W.-D. Hardt, and M. Doebeli. 2008. Self-destructive cooperation mediated by phenotypic noise. Nature 454:987–990.

Desnitskiy, A. G. 2016. Major ontogenetic transitions during Volvox (Chlorophyta) evolution: when and where might they have occurred? Dev. Genes Evol., doi: 10.1007/s00427-016-0557-0.

Matt, G., and J. Umen. 2016. Volvox: A simple algal model for embryogenesis, morphogenesis and cellular differentiation. Dev. Biol., doi: 10.1016/j.ydbio.2016.07.014.

Nedelcu, A. M., W. W. Driscoll, P. M. Durand, M. D. Herron, and A. Rashidi. 2011. On the paradigm of altruistic suicide in the unicellular world. Evolution 65:3–20.

Olson, B. J. S. C., and A. M. Nedelcu. 2016. Co-option during the evolution of multicellularity and developmental complexity in the volvocine green algae. Curr. Opin. Genet. Dev. 39:107–115.

Rebolleda-Gómez, M., W. C. Ratcliff, J. Fankhauser, and M. Travisano. 2016. Evolution of simple multicellularity increases environmental complexity. bioRxiv, doi: 10.1101/067991.

Wahl, M. E. and Murray, A. W. 2016. Multicellularity makes somatic differentiation evolutionarily stable. PNAS 113:8362–8367.

Comments

  1. grahamjones says

    ” Of course, it’s easy to say we shouldn’t be surprised after the fact; I’m not aware of anyone predicting this would happen before the fact (I certainly didn’t).”

    Evolutionary game theorists could have done, I think. But I don’t know if they actually did.

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