Actually, I fail to see a single thing in this paper that would require any textbook rewriting at all


Something about this title, “Evolutionary discovery to rewrite textbooks”, put me on edge. It’s a common trope to announce that your specific discovery is going to revolutionize everything, therefore you deserve more attention and glory and grant money. (Creationists seem not to understand this dynamic, though — they think scientists stick with the safe, and they think wrong, theory for all the money, when everyone knows a good, robust insight that changes minds is where the glory lies).

It’s in phys.org, though, which is generally a garbage fire of badly butchered summaries of papers, so that fact alone primes me to think the summary writer didn’t really understand the paper.

But then, it quotes the study author.

“This technology has been used only for the last few years, but it’s helped us finally address an age-old question, discovering something completely contrary to what anyone had ever proposed.”

“We’re taking a core theory of evolutionary biology and turning it on its head,” she said.

“Now we have an opportunity to re-imagine the steps that gave rise to the first animals, the underlying rules that turned single cells into multicellular animal life.”

Professor Degnan said he hoped the revelation would help us understand our own condition and our understanding of our own stem cells and cancer.

Aaaargh, no. They’re claiming that multicellular animals did not evolve from a single-celled ancestor resembling a choanoflagellate, a small protist with a single, prominent flagellar “propellor”, which many scientists consider to resemble one of the cells of sponges, called choanocytes. The idea is that the first multicellular animal would have arisen from colonies of choanoflagellates ganged together, with specialization of other cell types evolving later.

It’s fine and interesting that these investigators are proposing an alternative model, but this is not a “core theory of evolutionary biology”. It’s a likely hypothesis for the origin of a lineage of organisms we selfishly consider important, because it includes us, but it doesn’t actually revolutionize any part of the theory of evolution. Way too many scientists fail to grasp that there are the theories of evolution, that explain general mechanisms of the process, and that there are a multitude of facts of evolution, which are the instances in history that led to the specific distribution of evolutionary outcomes.

It’s like how there are physics theories that explain general phenomena: your car operates on all kinds of rules about force and acceleration and combustion. If you one day discover a shortcut on your commute to work, it may be an important personal discovery, but you don’t get to crow triumphantly about turning a core theory of automotive engineering and mechanics on its head.

But then, this is phys.org…I guess I’d better read the original paper.

It really is an interesting paper. It looks at the transcriptome of different cell types in sponges and compares them to the transcriptome of a choanoflagellate, and is basically addressing the reliability of a conclusion drawn from an observed phenotype, versus a conclusion drawn from patterns of gene expression. It’s going to argue that gene expression ought to be more fundamental, and I can sort of agree (while also seeing some problems of interpretation), but it then leaps to evolutionary conclusions from cell types, which I don’t find persuasive at all.

To summarize briefly: there are roughly three cell types in a sponge: 1) the choanocytes, which are flagellar motors that drive water flow through the animal; 2) pinacocytes, which form epithelial sheets that line the outside and insides; and 3) archaeocytes, which are found in a gooey mesenchymal smear between the layers of pinacocytes. A sponge is kind of sandwich, where the pinacocytes form the bread, the archaeocytes are the jelly, and the choanocytes are…damn, my analogy is breaking down. The choanocytes are imbedded in the bread and stir the surroundings.

The question then is, what genes are being expressed in these three cell types? And the answer is, well, lots of genes, and many of them are being differentially expressed — that is, there are genes unique to each cell type that reflect their general role.

We find that archaeocytes significantly upregulate genes involved in the control of cell proliferation, transcription and translation, consistent with their function as pluripotent stem cells. By contrast, choanocyte and pinacocyte transcriptomes are enriched for suites of genes that are involved in cell adhesion, signalling and polarity, consistent with their role as epithelial cells.

Now though, they raise an evolutionary question. They identify all these genes, and then ask which are common to single celled eukaryotes, which are common to multicellular animals, and which are unique to sponges. This gives a rough estimate of the evolutionary age of these genes; the first category is the oldest, found in pre-metazoan organisms, the second category may have arisen at the approximate time of origin of the metazoan lineage, and the third category would have appeared later as the sponge lineage specialized. They determined the relative contributions of these three categories to the patterns of gene expression in the three cell types.

The A. queenslandica [the sponge species] genome comprises 28% pre-metazoan, 26% metazoan and 46% sponge-specific protein-coding genes. We find that 43% of genes significantly upregulated in choanocytes are sponge-specific, which is similar to the proportion of the entire genome that is sponge-specific. By contrast, 62% of genes significantly upregulated in the pluripotent archaeocytes belong to the evolutionarily oldest pre-metazoan category, significantly higher than the 28% of genes for the entire genome. As with archaeocytes, pinacocytes express significantly more pre-metazoan and fewer sponge-specific genes than would be expected from the whole-genome profile.

Does this diagram help interpret that?

a, Phylostratigraphic estimate of the evolutionary age of coding genes in the A. queenslandica genome. b–d, Estimate of gene age of differentially expressed genes in choanocytes (b, top), archaeocytes (c, top) and pinacocytes (d, top) and the enrichment of phylostrata relative to the whole genome (b–d, bottom). Asterisks indicate significant difference (two-sided Fisher’s exact test P <0.001) from the whole genome. The enrichment values (log-odds ratio) for: choanocytes (b; n = 10) are sponge-specific (−0.0089, P = 0.7747), metazoan (–0.0361, P = 0.9958) and premetazoan (0.0439, P = 0.0004) genes; archaeocytes (c; n = 15) are sponge-specific (−0.5634, P = 1.33 × 10−133), metazoan (−0.1923, P = 1.04 × 10−18) and premetazoan (0.6772, P = 0); and pinacocytes (d; n = 6) are sponge-specific (−0.2173, P = 5.23 × 10−13), metazoan (−0.0008, P = 0.5231) and premetazoan (0.2359, P = 3.07 × 10−36).

OK, maybe not. Shorter summary: archaeocytes express lots of old genes, which makes sense, given we already had it explained that they’re enriched for genes involved in control of cell proliferation, transcription and translation, which are also ancient, primitive functions. Pinacocytes are also doing fairly basic things, and like the archaeocytes, are switching on basic essential genes. The choanocytes, though, are exceptional, and are turning on lots of sponge-specific genes that evolved after sponges diverged from other metazoans. The conclusion: choanocytes are switching on derived spongey genes that evolved for a spongey lifestyle, while archaeocytes are more generic, switching on a universal toolkit for adaptable stem cells, which have to be able to change their roles to become any of the three cell types.

They also make the point that the choanoflagellate gene expression pattern is most similar to that of the archaeocytes. From these observations, they argue that the ancestral metazoan more resembled a stem cell, like an archaeocyte, than a choanoflagellate.

…we posit that the ancestral metazoan cell type had the capacity to exist in and transition between multiple cell states in a manner similar to modern transdifferentiating and stem cells. Recent analyses of unicellular holozoan genomes support this proposition, with some of the genomic foundations of pluripotency being established deep in a unicellular past. Genomic innovations unique to metazoans—including the origin and expansion of key signalling pathway and transcription factor families, and regulatory DNA and RNA classes—may have conferred the ability of this ancestral pluripotent cell to evolve a regulatory system whereby it could co-exist in multiple states of differentiation, giving rise to the first multicellular animal.

And that’s where they lose me. I don’t buy their interpretation.

First, organisms do not evolve by descent from cell types. The whole genome is passed down. That choanocytes express a certain subset of genes is irrelevant — they carry the whole suite of genes, as do the pinacocytes and archaeocytes. You wouldn’t do a gene expression profile of human brain cells and compare it to the profile for mesenchymal cells, and then argue that brain cells are weird and unique, therefore we didn’t evolve from brain cells. Of course we didn’t! Your assumptions make no sense.

Second, what they found was that choanoflagellates exhibit a broader, more general pattern of gene expression than sponge choanocytes. This makes sense. Sponges are truly multicellular, with specialized subsets of cells that carry out specific roles, while choanoflagellates are unicellular, where each cell has to be a jack-of-all-trades. Yes, a choanoflagellate is going to have to use all of its genes, while individual cells in the sponge have the luxury of focusing on a smaller set of jobs. Choanocytes are specialized, they’re going to have a different expression profile than a generalist cell.

Third, choanoflagellates have an expression profile similar to an archaeocyte…but this is not in contradiction to their phenotype of having a flagellar collar. The metazoan ancestor could still have been a choanocyte, and nothing in this evidence contradicts that possibility!

All they’re really saying when you get right down to it is that metazoan ancestor had to have the capacity to generate diverse cell types later in its evolution, which is kind of obvious. They’re also arguing that the ancestral metazoan could not have been as locked in and limited in its repertoire of functions as a choanocyte in an extant sponge, which, again, is a given. What is not obvious is that the ancestor had to have been archaeocyte-like in form and function.

I also get the impression that the authors have been soaking in the transcriptomics literature and practice to the extent that they’ve lost sight of the bigger picture. They’d only have an argument if descendant forms were derived from the RNA of their ancestors…which actually would revolutionize the theory of evolution! Fortunately, they are not making that claim at all.


Sogabe S, Hatleberg WL, Kocot KM, Say TE, Stoupin D, Roper KE, Fernandez-Valverde SL, Degnan SM & Degnan BM (2019) Pluripotency and the origin of animal multicellularity. Nature https://doi.org/10.1038/s41586-019-1290-4

Comments

  1. garnetstar says

    All I can say is, whether one’s discovery is a revolutionary advance or not, it is a mighty bad idea to make such inflamed statements to the press. That’s never going to lead to anything good.

  2. blf says

    The nonsense about rewriting textbooks reminds me of when Pluto was re-classified as a dwarf planet. At least one dead-tree edition newspaper headline(?) was very similar to Astronomy Textbooks Must Be Urgently Rewritten. (The article itself was, as I now recall, Ok, this was another case of the subeditor(?) who composed the headline not having a clew and/or seemingly not having read the story carefully — I don’t (now) even recall textbooks being mentioned in the story!)

  3. kome says

    Shouldn’t it be up to the rest of the scientific community to determine whether your research is revolutionary or not? Of course we all would love it if our results helped advance our understanding of nature in leaps and bounds, but we are the last people in the world who should be making those claims.We’re far more biased to think our results are important than independent researchers’ should be biased towards skepticism of our results. At the very least, wait until independent labs have replicated your findings before touting how awesome-sauce your research is.

  4. monad says

    Wait, so is the idea that the single-celled organisms that feed with flagellate collars just like choanocytes, and which do in fact turn out to be the closest relatives of animals, only resemble them by convergence? I’m all for checking assumptions, but that seems like a pretty extraordinary claim to me, one that would need a lot of evidence.

    The article does mention two sources that found differences in their structure, but as another recent paper points out, homologous structures don’t need to be identical. And as far as I can tell, few or no other protists have developed something similar, which makes it suspicious.

  5. leerudolph says

    phys.org, which is generally a garbage fire

    I had never looked at phys.org; reading this, I visited its homepage but couldn’t find any “about” link, and was repelled by the overbusy layout, so I looked it up on Wikipedia (I know, sometimes that’s a matter of out of the garbage-fire, into the garbage, but not always) and found a succinctly snarky summary: “much of the content is republished directly from press releases and news agencies-in a practice known as churnalism.[1][2][3] It also produces some science journalism.[4][5].” Okay, I think I can continue to do without it…

  6. nomdeplume says

    Interesting post PZ, thank you. The single cell-multicellular development is one of the many fascinating turning pints in evolution. But I agree with you “rewrites the textbooks” is one of my pet hates (I have many pets) – it could only be said by someone who has never read a textbbok. But a question – I have always thought that sponges were an evolutionary side branch. Is the implication of the work here, and your comments, that sponges are on the main evolutionary line, ie that later multicellular organisms evolved from sponge ancestors?

  7. nomdeplume says

    Sorry, I missed this phrase on first reading “appeared later as the sponge lineage specialized”, which answers my question. But the second reading clarified my concern – archaeocytes in sponges are the way they are because of the role they fill in sponges. This tells you nothing about what the ancestral single cell looks or functions like (yes, this is just another way, I think, of saying what PZ said). I am reminded of another of my pet hates – finding single celled organisms in extreme environments on Earth and saying that this means life could evolve in similar extremes (of heat, pressure, salt etc) elsewhere in the universe. But the organisms on Earth are the fringe elements of the rich tapestry of life, only existing because of evolutionary pathways from organisms living in more favourable habitats. Their existence tells you nothing about life possibilities elsewhere.

  8. chrislawson says

    Textbooks are rewritten all the time. It’s not saying much, and I’m not even convinced that this particular finding is going to end up in textbooks anyway.

  9. chrislawson says

    nomdeplume@6:

    I think the evolution of fermentation was the key turning pint.

  10. John Harshman says

    Overhyped results are par for the course in Nature. In fact it helps you get in. Interesting stuff about sponge gene expression gets you into Cell, maybe.

  11. mountainbob says

    Thanks for the explication. I read the summary a couple days ago and was shaking my head, thinking that they were putting a lot of money on a questionable probability.

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