17 April 2013

Coelacanth genome surfaces

Unexpected insights from a fish with a 300-million-year-old fossil record

Phylogenetic tree of a selection of jawed vertebrates showing that lungfish, not coelacanth, is the closest relative of tetrapods.

Phylogenetic tree of a selection of jawed vertebrates showing that lungfish, not coelacanth, is the closest relative of tetrapods. [doi:10.1038/nature12027]

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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.

The team's study of the coelacanth genome confirms what many scientists had long suspected: genes in coelacanths are evolving more slowly than in other organisms. They also find intriguing suggestions of regions of the genome that helped in the move from sea to land.

A living coelacanth was discovered off the African coast in 1938 and, since then, the evolutionary position of these ancient-looking fish - popularly known as 'living fossils' - has been an enigma. Coelacanths today closely resemble the fossilised skeletons of their more than 300-million-year-old ancestors.

"We found that the genes overall are evolving significantly more slowly in the coelacanth than in every other fish and land vertebrate that we looked at," says Jessica Alföldi, a research scientist at the Broad Institute and co-first author of the 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.

"We often talk about how species have changed over time," says Kerstin Lindblad-Toh, scientific director of the Broad Institute's vertebrate genome biology group and senior author. "But there are still a few places on Earth where organisms don't have to change, and this is one of them. Coelacanths are likely very specialized to such a specific, non-changing, extreme environment - it is ideally suited to the deep sea just the way it is."

The coelacanth genome has also allowed scientists to test other long-debated questions. For example, coelacanths possess some features that look oddly similar to those seen only in animals that dwell on land, including 'lobed' fins, which resemble the limbs of four-legged land animals (known as tetrapods). Another odd-looking group of fish known as lungfish possesses lobed fins too. The genomes of these species suggest that the lungfish is more closely related to the tetrapod - and ultimately the human - ancestor.

A genome is not a dead and dry set of instructions, but a lens into the past and into the future," says Dr Steve Searle from the Wellcome Trust Sanger Institute. "We can glimpse the past and the distance travelled to today only because of our careful gene descriptions, our annotation. The gene structures we describe are the genomic skeleton for this 'living-fossil' fish, bearing marks of past history and presaging new developments in evolution.

" A genome is not a dead and dry set of instructions, but a lens into the past and into the future. "

Dr Steve Searle

"Through these gene descriptions, we see hints of the march from sea to land that occurred perhaps 400 million years ago."

Because of their resemblance to fossils dating back millions of years, coelacanths today are often referred to as 'living fossils' - a term coined by Charles Darwin. But the coelacanth is not a relic of the past brought back to life: it is a species that has survived, reproduced, but changed very little in appearance for millions of years.

However, the coelacanth is still a critical organism to study in order to understand what is often called the water-to-land transition. Lungfish may be more closely related to land animals, but its genome remains inscrutable: at 100 billion genetic letters in length, the lungfish genome is simply too unwieldy for scientists to sequence, assemble, and analyse. The coelacanth's more modest-sized genome (comparable in length to our own) is yielding valuable clues about the genetic changes that may have allowed tetrapods to flourish on land.

The researchers made several unusual discoveries by looking at which genes were lost when vertebrates came on land as well as changes to regulatory elements that govern where, when, and to what extent genes are active. For example, they found changes to regulatory regions controlling genes involved in sense of smell, the recruitment of several regulatory regions that were used by tetrapods to drive limb development and changes to a gene that specifies a key protein involved in the urea cycle - part of the excretion process that land animals use, whereas fish do not.

"This is just the beginning of many analyses on what the coelacanth can teach us about the emergence of land vertebrates, including humans, and, combined with modern empirical approaches, can lend insights into the mechanisms that have contributed to major evolutionary innovations," says Chris Amemiya, a member of the Benaroya Research Institute, professor at the University of Washington and co-first author of the paper.

Coelacanths are an endangered species, meaning that each sample obtained was precious. But the difficulties in obtaining a sample and the challenges of sequencing it also knitted the community together.

"The international nature of the work, its evolutionary value and history, and the fact that it was a technically challenging project really brought people together," continues Lindblad-Toh. "We had representatives from every populated continent on earth working on this project."

Although its genome offers some tantalising answers, the research team anticipates that further study of the fish's immunity, respiration, physiology, and more will lead to deep insights into how some vertebrates adapted to life on land, while others remained creatures of the sea.

Notes to Editors

Publication details

  • The African coelacanth genome provides insights into tetrapod evolution.

    Amemiya CT, Alföldi J, Lee AP, Fan S, Philippe H, Maccallum I, Braasch I, Manousaki T, Schneider I, Rohner N, Organ C, Chalopin D, Smith JJ, Robinson M, Dorrington RA, Gerdol M, Aken B, Biscotti MA, Barucca M, Baurain D, Berlin AM, Blatch GL, Buonocore F, Burmester T, Campbell MS, Canapa A, Cannon JP, Christoffels A, De Moro G, Edkins AL, Fan L, Fausto AM, Feiner N, Forconi M, Gamieldien J, Gnerre S, Gnirke A, Goldstone JV, Haerty W, Hahn ME, Hesse U, Hoffmann S, Johnson J, Karchner SI, Kuraku S, Lara M, Levin JZ, Litman GW, Mauceli E, Miyake T, Mueller MG, Nelson DR, Nitsche A, Olmo E, Ota T, Pallavicini A, Panji S, Picone B, Ponting CP, Prohaska SJ, Przybylski D, Saha NR, Ravi V, Ribeiro FJ, Sauka-Spengler T, Scapigliati G, Searle SM, Sharpe T, Simakov O, Stadler PF, Stegeman JJ, Sumiyama K, Tabbaa D, Tafer H, Turner-Maier J, van Heusden P, White S, Williams L, Yandell M, Brinkmann H, Volff JN, Tabin CJ, Shubin N, Schartl M, Jaffe DB, Postlethwait JH, Venkatesh B, Di Palma F, Lander ES, Meyer A and Lindblad-Toh K

    Nature 2013;496;7445;311-6

Funding

This work was supported by the African Coelacanth Ecosystem Programme of the South African National Department of Science and Technology, the National Human Genome Research Institute (NHGRI), the European Science Foundation. Additional contributions were made by the Genomics Sequencing Platform of the Broad Institute, the Association pour le Protection de Gombesa and other agencies.

A full list of funding can be found in the paper on the Nature website.

Participating Centres

A full list of participating centres can be found in the paper on the Nature website.

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