Coelacanths Evolve More Slowly?

I don't have a lot of time today (I leave for Boston tomorrow) but I can't let this pass.

The complete draft genome of the African coelacanth, Latimeria chalumnae has just been published in Nature (Amemiya et al. 2013). Ceolacanths have long been regarded as "living fossils," a term that persists even though the data have been disputed ever since the first fish were identified 75 years ago. I couldn't believe what I was reading when I saw the press release from the Broad Institute in Boston [Coelacanth genome surfaces]. The author, Haley Bridger of Broad Communications, says ...

An international team of researchers has decoded the genome of a creature whose evolutionary history is both enigmatic and illuminating: the African coelacanth. A sea-cave dwelling, five-foot long fish with limb-like fins, the coelacanth was once thought to be extinct. A living coelacanth was discovered off the African coast in 1938, and since then, questions about these ancient-looking fish – popularly known as “living fossils” – have loomed large. Coelacanths today closely resemble the fossilized skeletons of their more than 300-million-year-old ancestors. Its genome confirms what many researchers had long suspected: genes in coelacanths are evolving more slowly than in other organisms.

“We found that the genes overall are evolving significantly slower than in every other fish and land vertebrate that we looked at,” said Jessica Alföldi, a research scientist at the Broad Institute and co-first author of a paper on the coelacanth genome, which appears in Nature this week. “This is the first time that we’ve had a big enough gene set to really see that.”

Researchers hypothesize that this slow rate of change may be because coelacanths simply have not needed to change: they live primarily off of the Eastern African coast (a second coelacanth species lives off the coast of Indonesia), at ocean depths where relatively little has changed over the millennia.

This can't be right, I said to myself. Let's check out the actual paper.

Unfortunately, it was right. Here's the figure and here's what the authors say in the results section of the paper.

The morphological resemblance of the modern coelacanth to its fossil ancestors has resulted in it being nicknamed ‘the living fossil.’ This invites the question of whether the genome of the coelacanth is as slowly evolving as its outward appearance suggests. Earlier work showed that a few gene families, such as Hox and protocadherins, have comparatively slower protein-coding evolution in coelacanth than in other vertebrate lineages. To address the question, we compared several features of the coelacanth genome to those of other vertebrate genomes.

Protein-coding gene evolution was examined using the phylogenomics data set described above (251 concatenated proteins) (Fig. 1). Pair-wise distances between taxa were calculated from the branch lengths of the tree using the two-cluster test proposed previously to test for equality of average substitution rates. Then, for each of the following species and species clusters (coelacanth, lungfish, chicken and mammals), we ascertained their respective mean distance to an outgroup consisting of three cartilaginous fishes (elephant shark, little skate and spotted catshark). Finally, we tested whether there was any significant difference in the distance to the outgroup of cartilaginous fish for every pair of species and species clusters, using a Z statistic. When these distances to the outgroup of cartilaginous fish were compared, we found that the coelacanth proteins that were tested were significantly more slowly evolving (0.890 substitutions per site) than the lungfish (1.05 substitutions per site), chicken (1.09 substitutions per site) and mammalian (1.21 substitutions per site) orthologues (P < 10−6 in all cases) (Supplementary Data 5). In addition, as can be seen in Fig. 1, the substitution rate in coelacanth is approximately half that in tetrapods since the two lineages diverged. A Tajima’s relative rate test confirmed the coelacanth’s significantly slower rate of protein evolution (P < 10⁻²⁰)

The authors make it clear in the discussion that they think of molecular evolution of amino acid sequences only in terms of adaptation.

Since its discovery, the coelacanth has been referred to as a ‘living fossil’, owing to its morphological similarities to its fossil ancestors. However, questions have remained as to whether it is indeed evolving slowly, as morphological stasis does not necessarily imply genomic stasis. In this study, we have confirmed that the protein-coding genes of L. chalumnae show a decreased substitution rate compared to those of other sequenced vertebrates, even though its genome as a whole does not show evidence of low genome plasticity. The reason for this lower substitution rate is still unknown, although a static habitat and a lack of predation over evolutionary timescales could be contributing factors to a lower need for adaptation. A closer examination of gene families that show either unusually high or low levels of directional selection indicative of adaptation in the coelacanth may provide information on which selective pressures acted, and which pressures did not act, to shape this evolutionary relict.

This extraordinary claim flies in the face of everything we know about molecular evolution. Preliminary data from some of these same authors was criticized by Casane and Laurenti1 (2013) earlier this year. I'll quote what they said and leave it up to Sandwalk readers to draw their own conclusions.

Transposing the concept of ‘living fossil’ to the genomic level has led to the hypothesis of genetic stasis (or at least to the idea of a reduced molecular evolutionary rate) that is in sharp contrast with the principles of evolutionary genetics. Genomes change continuously under the combined effects of various mutational processes, that produce new variants, and genetic drift and selection, that eliminates or fixes them in populations. In other terms, the only possibility for genomes to replicate without change implies at least one of the two following conditions: (i) new variants do not appear (i.e. no mutations), and (ii) new variants are systematically eliminated by selection (i.e. no genetic drift and very powerful selection against new variants). Of course we can consider a less extreme case, i.e. a reduced evolutionary rate of the genome, but this still implies a lower mutation rate and/or stronger selection against new variants than observed in other species.

The coelacanth data make no sense. You should be very skeptical.

You should also wonder about the kind of people that Nature asks to review their papers. Reviewers may not be inclined to challenge the data but they should challenge the conclusions and they should ask the authors to address the fact that their interpretation is inconsistent with the modern evolutionary theory.

One other thing, if you look through the names of the authors, you will see several people who should know better than to attach their name to a paper like this. What's going on?

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[Photo Credit: This is a photo of a model of a related species Latimeria chalumnae from the Oxford University Museum. (Wikipedia)]

Amemiya, C.T. et al. (2013) The African coelacanth genome provides insights into tetrapod evolution. Nature 496:311–316. [doi: 10.1038/nature12027]

Casane, D. and Laurenti, P. (2013) Why coelacanths are not ‘living fossils.’ BioEssays 35:332-338. [doi: 10.1002/bies.201200145]

Posted in: Evolutionary Biology, Genome