Why do some fishes hybridize, while others don’t? A recent collaborative study with the University of Sydney, Australian Museum and University of Queensland, has asked this question of marine angelfishes. They found that hybridisation of these fishes is more widespread than previously thought...

The marine angelfishes are among the most iconic and charismatic of the coral reef fishes. Recent studies have suggested that hybridisation between species in this family are more prevalent than previously thought, with nearly 50% of all recognised species capable of forming hybrids. This makes the marine angelfishes among the groups of coral reef fishes with the highest incidences of hybridisation, with marine butterflyfishes previously holding the record.


Hybrids of marine angelfishes

Hybrids of marine angelfishes are often easily recognized due to their striking coloration. Offspring with hybrid ancestry often have varying levels of intermediate coloration patterns aligning with both parent species.

Image: Yi-Kai Tea
© Yi-Kai Tea

In the watery realm of coral reefs, where tangible barriers of isolation are few, hybridisation is not an uncommon phenomenon. While research in this field has expanded significantly over the years, hybridisation in the context of coral reefs remains enigmatic. Over 170 species of fishes are known to hybridise, but the factors limiting and permitting hybridisation are not fully understood.

The butterflyfishes have previously held the record for being the family with the highest incidences of hybridisation, with up to 39% species capable of forming hybrids. Although hybrids have been reported to occur throughout our ocean’s reefs, studies have shown that prevalence of reef fish hybrids are innately linked to certain biogeographical provinces – in particular along suture zones, where regions housing distinct fauna meet.

These “hybrid hotspots” bring together closely related species at the edges of their distributions, promoting interspecies pair formation and subsequent hybridisation. A recent survey of hybridisation events in the marine angelfishes however suggests a different scenario. We find that in contrast to the butterflyfishes (and most other reef fishes), marine angelfish hybrids are not constrained and limited to regional hotspots, where species narrowly overlap. Instead, they occur widely between sympatric species, i.e., species that overlap entirety within their ranges.


A juvenile Pomacanthus imperator x P. annularis hybrid

A juvenile Pomacanthus imperator x P. annularis hybrid with striking intermediate patterns.

Image: Yi-Kai Tea
© Yi-Kai Tea

One possible explanation for this lies in the inherent biology of the marine angelfishes. Unlike butterflyfishes, where monogamy and pair-bonding are common, many marine angelfishes are haremic, with several individuals living in social groups where males are outnumbered by females. The combination of haremic social structures, occurrence of mixed-species assemblages, and external broadcast spawning, likely contributes to the greater occurrence of sympatric hybrids in this family than in any other.

Our study reveals that hybridisation occurs in all but one genus of marine angelfishes, with close to 50% of all species capable of forming hybrids. Interestingly, hybridisation was reported to occur even between species that are deeply divergent and separated by more than 10% genetic distance in mitochondrial DNA, and over 10 million years of evolutionary time. This is remarkable, considering that hybrids are rarely known to occur between species that differ in more than 2–6% in mitochondrial DNA


Advances in molecular techniques of hybrid identification - Paracentropyge venusta x P. multifasciata

Advances in molecular techniques have made hybrid identification much easier, though identification of unilateral maternal inheritance of mitochondrial DNA. The squiggly hybrid of Paracentropyge venusta x P. multifasciata here has maternal ancestry from P. multifasciata. This remarkable hybrid is known from few museum specimens, with the Australian Museum Research Institute housing two species (AMS I. 48937­–001 and AMS I. 48938–001).

Image: Y.K. Tea, H. Senou, and J. Williams
© Y.K. Tea, H. Senou, and J. Williams

While we show that hybridisation in this group is more prevalent than previously thought, much remains unanswered, particularly in the context of why and how hybrids are formed. We still don’t know why some species hybridise and others don’t. For example, the regal angelfish, Pygoplites diacanthus, is found throughout the Indian and Pacific Oceans, yet no hybrids have ever been reported for this species. In terms of cracking the secrets to hybridisation in coral reefs, we’ve only just scratched the surface.


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


Acknowledgements:

We thank Amanda Hay, Kerryn Parkinson, and Meagan Warwick for curatorial and editorial assistance pertaining to this study. We thank Y.Z. Tay, J. K. Ong, and S.K. Tea for assisting with photographs used in this article.

Yi-Kai Tea was funded by a Research Training Program Scholarship from the Australian Government and an Australian Museum Foundation / Australian Museum Research Institute Fellowship.

Jean-Paul Hobbs was funded by the Australian Research Council (grant no. DE200101286). Joseph DiBattista was funded by a Curtin University Early Career Research Fellowship. Simon Ho and Nathan Lo were funded by the Australian Research Council (grant nos FT160100167 and FT160100463, respectively).


Reference:

Tea YK, Hobbs JPA, Vitelli F, DiBattista JD, Ho SYW, Lo N. 2020 Angels in disguise: sympatric hybridization in the marine angelfishes is widespread and occurs between deeply divergent lineages. Proceedings of the Royal Society B: 20201459. https://doi.org/10.1098/rspb.2020.1459


More information:

  • DiBattista JD, Whitney J, Craig MT, Hobbs JPA, Rocha LA, Feldheim KA, Berumen ML, Bowen BW. 2016. Surgeons and suture zones: hybridization among four surgeonfish species in the indo-Pacific with variable evolutionary outcomes. Molecular Phylogentics and Evolution, 101: 203–215.
  • Montanari SR, van Herwerden L, Pratchett MS, Hobbs JPA, Fugedi A. 2011. Reef fish hybridization: lessons learnt from butterflyfishes (genus Chaetodon). Ecology and Evolution, 2: 310–328.
  • DiBattista JD, Waldrop E, Bowen BW, Schultz JK, Gaither MR. Pyle RL, Rocha LA. 2012. Twisted sister species of pygmy angelfishes: discordance between taxonomy, colouration, and phylogenetics. Coral Reefs, 31: 839–851.
  • Coleman RR, Gaither MR, Kimokeo B, Stanton F, Bowen BW, Toonen RJ. 2014. Large-scale introduction of the Indo-Pacific damselfish Abudefduf vaigiensis into hawai’I promotes genetic swapping of the endemic congener A. abdominalis. Molecular Ecology, 23: 5552–5565.
  • University of Sydney, 4 August 2020. Angels in disguise: Angelfishes hybridize more than any other coral reef species. Phys.Org https://phys.org/news/2020-08-angels-disguise-angelfishes-hybridize-coral.html?deviceType=desktop