Coral reef fish diverged in ‘evolutionary arms race’ during last ice age

With their exuberant colours, fiery personalities and captivating courtshipdisplays, the fairy wrasses are one of the most beloved coral reef fish.Despite this, the evolutionary history of its genus was not well understood –until now.

Fairy wrasses diverged in form and colour after repeated sea level rises andfalls during the last ice age, finds a new study. Published in top journalSystematic Biology, it employed a novel genome-wide dataset to make thisdiscovery.

Lead author, ichthyologist and PhD candidate at the University of Sydney, MrYi-Kai (Kai) Tea, says that the fish’s divergence occurred rapidly and over ashort amount of time.

“Although the fairy wrasses split from their most common ancestor some 12million years ago, it was only within the last 2–5 million years ago that muchof their divergences took place, in the Pliocene/Pleistocene epoch,” said MrTea, a researcher in the School of Life and Environmental Sciences.

“They developed distinct colours and forms in a sort of evolutionary armsrace, putting on dazzling displays in an effort to court females and chase offrival males. Also, sea level changes caused groups to become isolated, andtherefore evolve separately. The repeated rise and fall of sea levels actedlike a ‘species pump’, propelling fish into the Indian Ocean and even as faras the Red Sea. Most of this movement, however, occurred in the Pacific Ocean,in particular, around the Indo-Australian Archipelago.”

Mr Tea completed the work under the supervision of Professors of MolecularEvolution, Simon Ho and Nathan Lo.

The most complete lineage of the fairy wrasses yet, with nearly 80 percent ofall species represented. Image: Yi-Kai Tea, Rudie Kuiter, Michael Hammer,Benjamin Victor, Gerry Allen and John Randall

Decoding fish DNA

Despite the vast variation in colour and form, many species of fairy wrasseshave highly conserved , or similar, regions of their genome. This poses achallenge in trying to reconstruct their evolutionary history.

The current study used an approach that had not been previously attempted onfairy wrasses: by combining genome-wide ultra-conserved elements withmitochondrial DNA, the researchers reconstructed a robust evolutionary tree.Using that, they began to tease apart the reason behind the fish’sdiversification.

An Australian species, the lavender-striped fairy wrasse, in ‘resting’ and‘flashing’ colouration. Image: Yi-Kai Tea

Do a little dance, make a little love

In addition to sea level fluctuations, male fairy wrasses (as with manyanimals, the more colourful sex) developed their bright colours and individualforms to court females.

“They do a little dance, and they are capable of changing colours, sometimestemporarily flashing bright, iridescent colours. They also do this to ward offrival males,” said Mr Tea. “In a reef where multiple species often occur,there is increased pressure for males to attract not only a female’sattention, but also the female of the correct species.”

“We have only just begun scratching the surface of this exciting group, andmore work still needs to be done in order to fully understand the drivers ofspecies diversification,” he continued.

That work, and the present study, might be germane to reef conservation andmanagement, too. For example, the finless ‘mutant wrasse’, an Australianendemic species restricted to a narrow distribution of reefs in far northwestWestern Australia, is listed as vulnerable on the International Union forConservation of Nature Red List of threatened species. The species has beenplaced in its own genus, with a single species. However, Mr Tea’s study findsstrong evidence that this species is simply a derived fairy wrasse, and thatits loss of fins likely resulted from it being ‘bottlenecked’ in a narrowarea.

The highly unusual Conniella apterygia is remarkable in lacking pelvic fins.This peculiar quality has earned it its common name, the Mutant Wrasse. Ourstudy finds strong evidence that Conniella apterygia is however, a derivedfairy wrasse, and that its loss of fins likely had something to do withpopulation bottlenecking as a result of its narrow distribution. Conniella ispresently known only from a few reefs off the northwestern coast of WesternAustralia. Image: Gerry Allen.

Fairy wrasse facts

**** Today, there are 61 fairy wrasse species, with new species continuallybeing discovered.

• Fairy wrasses are petite – they grow no larger than 15cm in length.
• They live in large groups in rubble reefs (dead coral and rocks), next to coral cover, at depths of 10 to 250 metres.
• Males are more colourful, larger, and often sport more ornamented fins than females (this is known as ‘sexual dimorphism’).
• Fairy wrasses are sequential hermaphrodites, meaning that females are capable of changing into fully functional males.
• Fairy wrasses were discovered in the mid 1800s, yet scientists only began to investigate their origins and evolutionary relationships in the last few decades.

Declaration: Yi-Kai Tea was funded by a Research Training ProgramScholarship from the Australian Government and by an Australian MuseumResearch Institute Postgraduate Award. Nathan Lo and Simon Ho were funded bythe Australian Research Council (FT160100463 and FT160100167). Peter Cowmanwas funded by an ARC DECRA Fellowship (DE170100516) and the ARC Centre ofExcellence Program (CE140100020).

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