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Twisted sister species of pygmy angelfishes: discordance between taxonomy, coloration, and phylogenetics

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Abstract

The delineation of reef fish species by coloration is problematic, particularly for the pygmy angelfishes (genus Centropyge), whose vivid colors are sometimes the only characters available for taxonomic classification. The Lemonpeel Angelfish (Centropyge flavissima) has Pacific and Indian Ocean forms separated by approximately 3,000 km and slight differences in coloration. These disjunct populations hybridize with Eibl’s Angelfish (Centropyge eibli) in the eastern Indian Ocean and the Pearl-Scaled Angelfish (Centropyge vrolikii) in the western Pacific. To resolve the evolutionary history of these species and color morphs, we employed mitochondrial DNA (mtDNA) cytochrome b and three nuclear introns (TMO, RAG2, and S7). Phylogenetic analyses reveal three deep mtDNA lineages (d = 7.0–8.3 %) that conform not to species designation or color morph but to geographic region: (1) most Pacific C. flavissima plus C. vrolikii, (2) C. flavissima from the Society Islands in French Polynesia, and (3) Indian Ocean C. flavissima plus C. eibli. In contrast, the nuclear introns each show a cluster of closely related alleles, with frequency differences between the three geographic groups. Hence, the mtDNA phylogeny reveals a period of isolation (ca. 3.5–4.2 million years) typical of congeneric species, whereas the within-lineage mtDNA ΦST values and the nuclear DNA data reveal recent or ongoing gene flow between species. We conclude that an ancient divergence of C. flavissima, recorded in the non-recombining mtDNA, was subsequently swamped by introgression and hybridization in two of the three regions, with only the Society Islands retaining the original C. flavissima haplotypes among our sample locations. Alternatively, the yellow color pattern of C. flavissima may have appeared independently in the central Pacific Ocean and eastern Indian Ocean. Regardless of how the pattern arose, C. flavissima seems to be retaining species identity where it interbreeds with C. vrolikii and C. eibli, and sexual or natural selection may help to maintain color differences despite apparent gene flow.

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Acknowledgments

This research was supported by the National Science Foundation grants OCE-0453167 and OCE-0929031 to BWB, NOAA National Marine Sanctuaries Program MOA No. 2005-008/66882 to R.J. Toonen, and by a Natural Sciences and Engineering Research Council of Canada (NSERC) postgraduate fellowship to JDD. For specimen collections, we thank Kim Andersen, Paul Barber, Larry Basch, David Bellwood, J. Howard Choat, Matthew Craig, Joshua Drew, John Earle, Jeff Eble, Brian Greene, Matthew Iacchei, Stephen Karl, Randall Kosaki, David Pence, and Ross Robertson. We thank Sue Taei at Conservation International, Graham Wragg of the RV Bounty Bay, the Government of Kiribati, including Tukabu Teroroko and the Phoenix Island Protected Area who assisted with Kiribati collections. We also thank Robert Toonen, Serge Planes, Stephen Karl, John Randall, Joann Leong, Patrick Colin, Laura Colin, the Coral Reef Research Foundation, and members of the ToBo lab for their logistic support; we thank the Center for Genomics, Proteomics, and Bioinformatics at the University of Hawaii for their assistance with DNA sequencing. This is contribution no. 1492 from the Hawai’i Institute of Marine Biology and no. 8605 from the School of Ocean and Earth Science and Technology.

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Authors and Affiliations

  1. Hawai’i Institute of Marine Biology, P.O. Box 1346, Kane’ohe, HI, 96744, USA

    Joseph D. DiBattista, Ellen Waldrop, Brian W. Bowen & Jennifer K. Schultz

  2. Section of Ichthyology, California Academy of Sciences, 55 Music Concourse Dr, San Francisco, CA, 94118, USA

    Michelle R. Gaither & Luiz A. Rocha

  3. Bernice P. Bishop Museum, 1525 Bernice St., Honolulu, HI, 96817, USA

    Richard L. Pyle

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  1. Joseph D. DiBattista
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  2. Ellen Waldrop
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  3. Brian W. Bowen
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Correspondence to Joseph D. DiBattista.

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DiBattista, J.D., Waldrop, E., Bowen, B.W. et al. Twisted sister species of pygmy angelfishes: discordance between taxonomy, coloration, and phylogenetics. Coral Reefs 31, 839–851 (2012). https://doi.org/10.1007/s00338-012-0907-y

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