A recent study with Yi-Kai Tea and Joey DiBattista at the Australian Museum uncovers the evolutionary origins of the most species-rich wrasse lineage with the help of an integrative genome-wide dataset.

Fairy wrasses (genus Cirrhilabrus) are among the most evolutionarily successful and captivating of the extant labrids, with their 61 species accounting for nearly 10% of the family. Yet previous attempts to resolve their evolutionary relationships have been unsuccessful. Using an integrative genome-wide dataset, we uncover the evolutionary history and patterns of diversification driving the evolutionary success of the fairy wrasses.


The fairy wrasses are among the most diverse of the Labridae, with their 61 species accounting for nearly 10% of the family. Photo credit: Yi-Kai Tea.

The fairy wrasses are among the most diverse of the Labridae, with their 61 species accounting for nearly 10% of the family.

Image: Yi-Kai Tea
© Yi-Kai Tea

With their exuberant colours, fiery personalities and captivating courtship displays, the fairy wrasses have captivated underwater photographers and aquarists alike. With a maximum length of just over 15 centimetres in the largest species, what the fairy wrasses lack in size they make up for in beauty and numbers.


New species of fairy wrasses, like the Vibranium Fairy Wrasse (Cirrhilabrus wakanda) are continuously being discovered every year. Photo credit: Luiz Rocha.

New species of fairy wrasses, like the Vibranium Fairy Wrasse (Cirrhilabrus wakanda), are continuously being discovered every year.

Image: Luiz Rocha
© Luiz Rocha

While fairy wrasses have been known to science since the mid 1800s, it is only in the last few decades that fairy wrasse taxonomy has really taken off. Presently, the genus has grown to accommodate 61 species, with many more new species discovered annually. These brightly coloured fishes live in large groups in low-complexity rubble reefs adjacent to coral cover, at depths ranging from 10 to 250 metres. Like all wrasses, the fairy wrasses are sequential hermaphrodites, meaning that females are capable of changing into fully functional males.

Yet for such a diverse group, with species found all over the Pacific and Indian Oceans, the evolutionary history of the fairy wrasses has been shrouded in mystery. Previous phylogenetic studies have been met with limited success, in part due to low sequence variation in mitochondrial DNA and the lack of informative morphological characters. Together, these factors have made the fairy wrasses among the more phylogenetically recalcitrant and intractable lineages to untangle.

Our recent study takes a new approach at resolving the evolutionary history of the fairy wrasses. Using a combined dataset, comprising of genome-wide ultraconserved elements and mitochondrial DNA representing 80% of all fairy wrasses, we are now beginning to understand the reason for their diversification.


The most taxonomically complete phylogenetic tree of the fairy wrasses yet, with nearly 80% of all species represented. Photo credit: Yi-Kai Tea, Rudie Kuiter, Michael Hammer, Benjamin Victor, Gerry Allen, and the late John Randall.

The most taxonomically complete phylogenetic tree of the fairy wrasses yet, with nearly 80% of all species represented.

Image: Yi-Kai Tea, Rudie Kuiter, Michael Hammer, Benjamin Victor, Gerry Allen, and the late John Randall.
© Yi-Kai Tea, Rudie Kuiter, Michael Hammer, Benjamin Victor, Gerry Allen, and the late John Randall.

The fairy wrasses shared a common ancestor about 9 million years ago during the late Miocene, with most of the deeper divergences occurring between 5.7–7.4 million years. These deeper Miocene divergences were succeeded by a series of cladogenetic events between 3.3–4.7 million years ago, with several species splitting from their closest relatives as recent as 100 thousand years ago. Biogeographical reconstruction indicates that most of these events took place within the Pacific Ocean, in particular, the Indo-Australian Archipelago. During the Pleistocene glacial cycles, this region would have been characterised by rapid expansion and contraction of sea levels. These fluctuating and oftentimes ephemeral barriers acted as sort of a species pump, by isolating and allowing populations to diversify and speciate from each other. Our study also indicates that the fairy wrasses underwent at least five independent incursions into the Indian Ocean, expanding outside of their Pacific Ocean centre of diversity.

There is also evidence to suggest that sexual selection has some part to play in the overarching evolutionary story of the fairy wrasses. We have only just begun scratching the surface of this exciting group, and more work still needs to be done in order to fully understand the drivers of speciation. For one, the rapid expansion occurring in short temporal scales during the last glacial cycle has made phylogenetic reconstruction challenging, with extensive discordance between gene trees and species trees.


The highly unusual Conniella apterygia is remarkable in lacking pelvic fins. This peculiar quality has earned it its common name, the Mutant Wrasse. Our study finds strong evidence that Conniella apterygia is however, a derived fairy wrasse, and that its

The highly unusual Conniella apterygia is remarkable in lacking pelvic fins. This peculiar quality has earned it its common name, the Mutant Wrasse. Our study finds strong evidence that Conniella apterygia is however, a derived fairy wrasse, and that its loss of fins likely had something to do with population bottlenecking as a result of its narrow distribution. Conniella is presently known only from a few reefs off the northwestern coast of Western Australia.

Image: Gerry Allen
© Gerry Allen

Nonetheless, this research provides exciting insights into one of the most spectacular groups of coral reef fishes, with important findings that may be of interest to species conservation and management. In particular, the highly unusual mutant wrasse (Conniella apterygia), an Australian endemic species restricted to a narrow distribution of reefs in far northwest Western Australia, is presently listed as vulnerable on the IUCN Red List of threatened species.


Yi-Kai Tea, PhD candidate, University of Sydney; 2019-20 AMF/AMRI Postgraduate Award Recipient, Australian Museum Research Institute.


Acknowledgements:

We thank Amanda Hay, Sally Reader, and Kerryn Parkinson of the Australian Museum for curatorial support. Gerald R. Allen (Western Australian Museum), David R. Bellwood (James Cook University), Michael P. Hammer (Museum and Art Gallery of the Northern Territory), Luiz A. Rocha (California Academy of Sciences), Kelvin Lim (Lee Kong Chian Natural History Museum), Benjamin C. Victor, and Fenton Walsh provided valuable tissue samples. All genetic materials obtained from museums were procured in accordance with guidelines and approval from the respective institutions. Tissue curation and DNA extractions were performed by Martina de Freitas Prazeres, Hillary Smith, and Julia Yun-Hsuan Hung. Benjamin W. Frable and Joseph Rowlett provided valuable discourse on the subject matter. Charles P. Foster and Kevin Love provided custom scripts for data handling. We dedicate this study to the late John Ernest Randall, who was a fierce and pioneering force in the modern age of ichthyology, and to Hiroyuki Tanaka, who has contributed significantly towards our understanding of the genus.

Yi-Kai Tea was funded by a Research Training Program Scholarship from the Australian Government and by an Australian Museum Research Institute Postgraduate Award. Nathan Lo and Simon Ho were funded by the Australian Research Council (FT160100463 and FT160100167). Peter Cowman was funded by an ARC DECRA Fellowship (DE170100516) and the ARC Centre of Excellence Program (CE140100020).


Reference:

Tea YK, Xu X, DiBattista JD, Lo N, Cowman PF, Ho SYW. 2021 Phylogenomic analysis of concatenated ultraconserved elements reveals the recent evolutionary radiation of the fairy wrasses (Teleostei: Labridae: Cirrhilabrus). Systematic Biology. https://doi.org/10.1093/sysbio/syab012