Evolution of pygmy angelfishes: Recent divergences, introgression, and the usefulness of color in taxonomy

dc.contributor.authorGaither, Michelle R.
dc.contributor.authorSchultz, Jennifer K.
dc.contributor.authorBellwood, David R.
dc.contributor.authorPyle, Richard L.
dc.contributor.authorDiBattista, Joseph
dc.contributor.authorRocha, Luiz A.
dc.contributor.authorBowen, Brian W.
dc.contributor.departmentRed Sea Research Center (RSRC)
dc.contributor.departmentMarine Science Program
dc.contributor.institutionCalif Acad Sci, Sect Ichthyol, San Francisco, CA 94118 USA
dc.contributor.institutionNOAA Fisheries, Silver Spring, MD 20910 USA
dc.contributor.institutionJames Cook Univ, Sch Marine & Trop Biol, Townsville, Qld, Australia
dc.contributor.institutionJames Cook Univ, ARC Ctr Excellence Coral Reef Studies, Townsville, Qld, Australia
dc.contributor.institutionBernice P Bishop Museum, Honolulu, HI 96817 USA
dc.contributor.institutionHawaii Inst Marine Biol, Kaneohe, HI 96744 USA
dc.date.accessioned2015-08-03T11:53:31Z
dc.date.available2015-08-03T11:53:31Z
dc.date.issued2014-05
dc.description.abstractThe pygmy angelfishes (genus Centropyge, family Pomacanthidae) are brightly colored species that occupy reef habitats in every tropical ocean. Some species are rarely observed because they occur below conventional scuba depths. Their striking coloration can command thousands of U.S. dollars in the aquarium trade, and closely related species are often distinguished only by coloration. These factors have impeded phylogenetic resolution, and every phylogeographic survey to date has reported discordance between coloration, taxonomy, and genetic partitions. Here we report a phylogenetic survey of 29 of the 34 recognized species (N= 94 plus 23 outgroups), based on two mtDNA and three nuclear loci, totaling 2272. bp. The resulting ML and Baysian trees are highly concordant and indicate that the genus Centropyge is paraphyletic, consistent with a previous analysis of the family Pomacanthidae. Two recognized genera (Apolemichthys and Genicanthus) nest within Centropyge, and two subgenera (Xiphypops and Paracentropyge) comprise monophyletic lineages that should be elevated to genus level. Based on an age estimate of 38. Ma for the family Pomacanthidae, Centropyge diverged from the closest extant genus Pygoplites about 33. Ma, three deep lineages within Centropyge diverged about 18-28. Ma, and four species complexes diverged 3-12. Ma. However, in 11 of 13 cases, putative species in these complexes are indistinguishable based on morphology and genetics, being defined solely by coloration. These cases indicate either emerging species or excessive taxonomic splitting based on brightly colored variants. © 2014 Elsevier Inc.
dc.description.sponsorshipFor specimen collections, valuable advice and logistic assistance we thank Senifa Annandale, Frank Baensch, Chris Bowen, John Coppolino, Joshua Copus, Matthew Craig, Edward DeMartini, John Earle, Jeff Eble, Jen Fessler, Brian Greene, David Greenfield, J.P. Hobbs, Shelley Jones, Stephen Karl, Nicolai Konow, Randy Kosaki, Mike Lameier, Ross Langston, Ken Longenecker, Marvin Lutneski, Carl Meyer, Gustav Pauley, Jason Philibotte, John Randall, D. Ross Robertson, Kang-Ning Shen, Charles Sheppard, Julian Sprung, Robert Thorn, Ellen Waldrop, Jimmy Young and Zoltan Szabo. We also thank Robert Toonen and members of the ToBo lab for logistic support, Moises Bernal, Claudia Rocha, Anna Sellas and Brian Simison at the California Academy of Sciences for support and lively discussions, and the Center for Genomics, Proteomics, and Bioinformatics at the University of Hawai'i for their assistance with DNA sequencing. This research was supported by National Science Foundation grants to BWB (most recently OCE-0929031), by the Seaver Institute, and by a Natural Sciences and Engineering Research Council of Canada (NSERC) postgraduate fellowship to JDD. MRG was supported by a fellowship from the University of Hawai'i Sea Grant College Program, SOEST, under Institutional Grant No. NA090AR4170060 from NOAA Office of Sea Grant, Department of Commerce and the California Academy of Sciences. DRB was supported by the Australian Research Council. Field work at Cocos/Keeling and Christmas Island (Indian Ocean) was supported by National Geographic Grant 8208-07 to Matthew T. Craig. This is contribution no. 1578 from the Hawaii Institute of Marine Biology, no. 9061 from the School of Ocean and Earth Science and Technology, and UNIHI-SEAGRANT-JC-11-22 from the University of Hawai'i Sea Grant Program.
dc.identifier.citationGaither, M. R., Schultz, J. K., Bellwood, D. R., Pyle, R. L., DiBattista, J. D., Rocha, L. A., & Bowen, B. W. (2014). Evolution of pygmy angelfishes: Recent divergences, introgression, and the usefulness of color in taxonomy. Molecular Phylogenetics and Evolution, 74, 38–47. doi:10.1016/j.ympev.2014.01.017
dc.identifier.doi10.1016/j.ympev.2014.01.017
dc.identifier.issn10557903
dc.identifier.journalMolecular Phylogenetics and Evolution
dc.identifier.pmid24500654
dc.identifier.urihttp://hdl.handle.net/10754/563520
dc.publisherElsevier BV
dc.subjectCentropyge
dc.subjectCoral reef fish
dc.subjectHybridization
dc.subjectIncomplete lineage sorting
dc.subjectMitochondrial DNA
dc.subjectNuclear introns
dc.titleEvolution of pygmy angelfishes: Recent divergences, introgression, and the usefulness of color in taxonomy
dc.typeArticle
display.details.left<span><h5>Type</h5>Article<br><br><h5>Authors</h5><a href="https://repository.kaust.edu.sa/search?query=orcid.id:0000-0002-0371-5621&spc.sf=dc.date.issued&spc.sd=DESC">Gaither, Michelle R.</a> <a href="https://orcid.org/0000-0002-0371-5621" target="_blank"><img src="https://repository.kaust.edu.sa/server/api/core/bitstreams/82a625b4-ed4b-40c8-865a-d6a5225a26a4/content" width="16" height="16"/></a><br><a href="https://repository.kaust.edu.sa/search?spc.sf=dc.date.issued&spc.sd=DESC&f.author=Schultz, Jennifer K.,equals">Schultz, Jennifer K.</a><br><a href="https://repository.kaust.edu.sa/search?spc.sf=dc.date.issued&spc.sd=DESC&f.author=Bellwood, David R.,equals">Bellwood, David R.</a><br><a href="https://repository.kaust.edu.sa/search?spc.sf=dc.date.issued&spc.sd=DESC&f.author=Pyle, Richard L.,equals">Pyle, Richard L.</a><br><a href="https://repository.kaust.edu.sa/search?query=orcid.id:0000-0002-5696-7574&spc.sf=dc.date.issued&spc.sd=DESC">DiBattista, Joseph</a> <a href="https://orcid.org/0000-0002-5696-7574" target="_blank"><img src="https://repository.kaust.edu.sa/server/api/core/bitstreams/82a625b4-ed4b-40c8-865a-d6a5225a26a4/content" width="16" height="16"/></a><br><a href="https://repository.kaust.edu.sa/search?spc.sf=dc.date.issued&spc.sd=DESC&f.author=Rocha, Luiz A.,equals">Rocha, Luiz A.</a><br><a href="https://repository.kaust.edu.sa/search?spc.sf=dc.date.issued&spc.sd=DESC&f.author=Bowen, Brian W.,equals">Bowen, Brian W.</a><br><br><h5>KAUST Department</h5><a href="https://repository.kaust.edu.sa/search?spc.sf=dc.date.issued&spc.sd=DESC&f.department=Red Sea Research Center (RSRC),equals">Red Sea Research Center (RSRC)</a><br><a href="https://repository.kaust.edu.sa/search?spc.sf=dc.date.issued&spc.sd=DESC&f.department=Marine Science Program,equals">Marine Science Program</a><br><br><h5>Date</h5>2014-05</span>
display.details.right<span><h5>Abstract</h5>The pygmy angelfishes (genus Centropyge, family Pomacanthidae) are brightly colored species that occupy reef habitats in every tropical ocean. Some species are rarely observed because they occur below conventional scuba depths. Their striking coloration can command thousands of U.S. dollars in the aquarium trade, and closely related species are often distinguished only by coloration. These factors have impeded phylogenetic resolution, and every phylogeographic survey to date has reported discordance between coloration, taxonomy, and genetic partitions. Here we report a phylogenetic survey of 29 of the 34 recognized species (N= 94 plus 23 outgroups), based on two mtDNA and three nuclear loci, totaling 2272. bp. The resulting ML and Baysian trees are highly concordant and indicate that the genus Centropyge is paraphyletic, consistent with a previous analysis of the family Pomacanthidae. Two recognized genera (Apolemichthys and Genicanthus) nest within Centropyge, and two subgenera (Xiphypops and Paracentropyge) comprise monophyletic lineages that should be elevated to genus level. Based on an age estimate of 38. Ma for the family Pomacanthidae, Centropyge diverged from the closest extant genus Pygoplites about 33. Ma, three deep lineages within Centropyge diverged about 18-28. Ma, and four species complexes diverged 3-12. Ma. However, in 11 of 13 cases, putative species in these complexes are indistinguishable based on morphology and genetics, being defined solely by coloration. These cases indicate either emerging species or excessive taxonomic splitting based on brightly colored variants. © 2014 Elsevier Inc.<br><br><h5>Citation</h5>Gaither, M. R., Schultz, J. K., Bellwood, D. R., Pyle, R. L., DiBattista, J. D., Rocha, L. A., & Bowen, B. W. (2014). Evolution of pygmy angelfishes: Recent divergences, introgression, and the usefulness of color in taxonomy. Molecular Phylogenetics and Evolution, 74, 38–47. doi:10.1016/j.ympev.2014.01.017<br><br><h5>Acknowledgements</h5>For specimen collections, valuable advice and logistic assistance we thank Senifa Annandale, Frank Baensch, Chris Bowen, John Coppolino, Joshua Copus, Matthew Craig, Edward DeMartini, John Earle, Jeff Eble, Jen Fessler, Brian Greene, David Greenfield, J.P. Hobbs, Shelley Jones, Stephen Karl, Nicolai Konow, Randy Kosaki, Mike Lameier, Ross Langston, Ken Longenecker, Marvin Lutneski, Carl Meyer, Gustav Pauley, Jason Philibotte, John Randall, D. Ross Robertson, Kang-Ning Shen, Charles Sheppard, Julian Sprung, Robert Thorn, Ellen Waldrop, Jimmy Young and Zoltan Szabo. We also thank Robert Toonen and members of the ToBo lab for logistic support, Moises Bernal, Claudia Rocha, Anna Sellas and Brian Simison at the California Academy of Sciences for support and lively discussions, and the Center for Genomics, Proteomics, and Bioinformatics at the University of Hawai'i for their assistance with DNA sequencing. This research was supported by National Science Foundation grants to BWB (most recently OCE-0929031), by the Seaver Institute, and by a Natural Sciences and Engineering Research Council of Canada (NSERC) postgraduate fellowship to JDD. MRG was supported by a fellowship from the University of Hawai'i Sea Grant College Program, SOEST, under Institutional Grant No. NA090AR4170060 from NOAA Office of Sea Grant, Department of Commerce and the California Academy of Sciences. DRB was supported by the Australian Research Council. Field work at Cocos/Keeling and Christmas Island (Indian Ocean) was supported by National Geographic Grant 8208-07 to Matthew T. Craig. This is contribution no. 1578 from the Hawaii Institute of Marine Biology, no. 9061 from the School of Ocean and Earth Science and Technology, and UNIHI-SEAGRANT-JC-11-22 from the University of Hawai'i Sea Grant Program.<br><br><h5>Publisher</h5><a href="https://repository.kaust.edu.sa/search?spc.sf=dc.date.issued&spc.sd=DESC&f.publisher=Elsevier BV,equals">Elsevier BV</a><br><br><h5>Journal</h5><a href="https://repository.kaust.edu.sa/search?spc.sf=dc.date.issued&spc.sd=DESC&f.journal=Molecular Phylogenetics and Evolution,equals">Molecular Phylogenetics and Evolution</a><br><br><h5>DOI</h5><a href="https://doi.org/10.1016/j.ympev.2014.01.017">10.1016/j.ympev.2014.01.017</a><br><br><h5>PubMed ID</h5><a href="https://www.ncbi.nlm.nih.gov/pubmed/24500654">24500654</a></span>
kaust.personDiBattista, Joseph
orcid.authorGaither, Michelle R.::0000-0002-0371-5621
orcid.authorSchultz, Jennifer K.
orcid.authorBellwood, David R.
orcid.authorPyle, Richard L.
orcid.authorDiBattista, Joseph::0000-0002-5696-7574
orcid.authorRocha, Luiz A.
orcid.authorBowen, Brian W.
orcid.id0000-0002-5696-7574
orcid.id0000-0002-0371-5621
Files