DNA sequence data shows that this "living fossil" isn't so fossilized after all

A nautilus, very much alive and not replaced by mineral accretions at all, thank you. (Flickr: muzina_shanghai)

Living fossils are a tricky concept for evolutionary biology. In principle it seems simple: living organisms that closely resemble creatures seen in the fossil record going back millions of years. Usually they’re a single representative of a fossil record containing a multitude of diverse close relatives — survivors from a lost clade — and rare, or living in habitats that humans can’t easily access. As a consequence, living fossils’ shared ancestry with other living species goes back deep into the history of life, and they’re often treated as examples of “primitive” forms. The term has been applied to species including the coelacanth, dawn redwoods, ginkgo trees, and hoatzin.
However, as molecular ecologists well know, two organisms may look identical in terms of morphology, especially features like shells and skeletons that fossilize reliably, and still be quite different in ways less obvious to the human eye. Color or pheromones or behavior may change without leaving any fossil traces; and every living thing is locked in an ongoing coevolutionary race against parasites and pathogens, which necessitates rapid evolution at the molecular level. We can’t find evidence of these changes in fossils (well, except for relatively very recent ones), but we can see it in DNA sequence data from putative living fossils.
That’s the premise of a paper out ahead of print in Molecular Ecology, which reports the first substantial, genome-wide population genetic dataset for nautiluses. Nautiluses are cephalopod mollusks, most closely related to octopuses, with beautiful spiral shells. Though there are five recognized species in two genera, they are collectively considered living fossils, as the fossil record includes species from at least five other genera, and all of them are different enough from other cephalopods to rate placement in a separate suborder, the Nautiloidea. David Combosh, Sarah Lemer, and colleagues at Harvard, the University of Guam, and the University of Washington collected genome-wide SNP data from 140 samples of all five species using the ddRADseq protocol, and used it to take the first good look at nautilus diversity.
What they found is a mess for nautilus taxonomy. Phylogenetic analysis of the concatenated SNP dataset revealed three major clades within the genus Nautilus, none of them corresponding well to the current species identities of the sequenced samples. All the Nautilus macromphalus samples did form a monophyletic grouping within one of the three major clades; but N. belauensis, N. repertus, and N. stenomphalus were scattered across the other two clades. Samples of N. pompilius, previously considered the most widespread species and the best represented in the dataset, were in all three clades. Analysis with STRUCTURE paralleled the phylogenetic result, and suggested ongoing gene flow between separate populations within the clades. (How do you get population structure in an oceanic species like these? Nautiluses hang out near reefs, where they can quickly hide from predators, and their shells apparently implode at pressures they’d encounter below depths of 800 meters, so they don’t often cross open ocean.)
The authors line up these analyses in a nice composite figure.

Combosch et al. suggest that, at a minimum, the population groupings revealed by STRUCTURE represent five separate species, and this hidden species diversity is one result from the genetic data that complicates the “living fossil” status of nautiluses. If we’ve done a poor job in understanding the taxonomic diversity of extant nautilus species, we may have done no better with the fossil ancestors that they resemble so closely. Another complication is the fact that genetic differentiation (FST) between population groupings is stronger at protein-coding genes than at non-coding loci, consistent with ongoing natural selection that differs between those populations — hardly a sign of evolutionary stasis. Finally, the authors used the SNP data to estimate effective population sizes for each of the three clades, and found that, historically, they’ve been quite large. Nautiluses are currently threatened by hunting for their shells, and the genetic data would likely not capture declines in the relatively recent past. But if their populations were larger and robust before humans took an interest in them, nautiluses may not have been the rare, marginalized survivors we think of when we think of living fossils.
These results should help plan the conservation of nautilus populations, and they expand our understanding of what exactly a living fossil is, or could be. Population genetic data for other putative living fossils is still quite sparse, but genomic sequencing of small samples has found unusually slow rates of DNA sequence evolution in parallel with the apparent morphological stasis of coelacanths, elephant sharks and painted turtles. The gingko genome seems to show quite a bit of structural evolution — but we don’t have data for variation within that species, yet.
What’s clear from the results for Nautilus is that applying genetic data to these edge-cases of evolution will likely reveal that there’s more going on than meets the eye.
Combosch DJ, S Lemer, PD Ward, NH Landman, and G Giribet. 2017. Genomic signatures of evolution in Nautilus – an endangered living fossil. Molecular Ecology. doi: 10.1111/mec.14344
De La Torre AR, Z Li, Y Van de Peer, and PK Ingvarsson. 2017. Contrasting rates of molecular evolution and patterns of selection among gymnosperms and flowering plants. Molecular Biology and Evolution, 34(6):1363-1377. doi: 10.1093/molbev/msx069
Guan R, Y Zhao, H Zhang, et al.. 2016. Draft genome of the living fossil Ginkgo biloba. GigaScience, 5(1): 49. doi: 10.1186/s13742-016-0154-1
Pallavicini A, A Canapa, M Barucca, J Alfőldi, MA Biscotti, F Buonocore, G De Moro, F Di Palma, AM Fausto, M Forconi, and M Gerdol. 2013. Analysis of the transcriptome of the Indonesian coelacanth Latimeria menadoensis. BMC Genomics, 14(1): 538. doi: 10.1186/1471-2164-14-538
Peterson BK, JN Weber, EH Kay, HS Fisher, HE and Hoekstra. 2012. Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PlOS ONE, 7(5), p.e37135. doi: 10.1371/journal.pone.0037135
Saunders WB and DA Wehman. 1977. Shell strength of Nautilus as a depth limiting factor. Paleobiology, 3(1):83-89. doi: 10.1017/S0094837300005133
Shaffer HB, P Minx, DE Warren, et al. 2013. The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage. Genome Biology, 14(3): R28. doi: 10.1186/gb-2013-14-3-r28
Venkatesh B, AP Lee, V Ravi, et al. 2014. Elephant shark genome provides unique insights into gnathostome evolution. Nature, 505(7482): 174. doi: 10.1038/nature12826

About Jeremy Yoder

Jeremy B. Yoder is an Associate Professor of Biology at California State University Northridge, studying the evolution and coevolution of interacting species, especially mutualists. He is a collaborator with the Joshua Tree Genome Project and the Queer in STEM study of LGBTQ experiences in scientific careers. He has written for the website of Scientific American, the LA Review of Books, the Chronicle of Higher Education, The Awl, and Slate.
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