Phylogeography of Indo-Pacific reef fishes: sister wrasses Coris gaimard and C. cuvieri in the Red Sea, Indian Ocean and Pacific Ocean
Corresponding Author
Pauliina A. Ahti
Hawai'i Institute of Marine Biology, University of Hawai'i, Kāne'ohe, HI, 96744 USA
School of Life Sciences, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, G12 8QQ UK
Correspondence: Pauliina A. Ahti, School of Life Sciences, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow G12 8QQ, UK.
E-mail: [email protected]
Search for more papers by this authorRichard R. Coleman
Hawai'i Institute of Marine Biology, University of Hawai'i, Kāne'ohe, HI, 96744 USA
Search for more papers by this authorJoseph D. DiBattista
Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology (KAUST), Thuwal, 23955-6900 Saudi Arabia
Department of Environment and Agriculture, Curtin University, PO Box U1987, Perth, WA, 6845 Australia
Search for more papers by this authorMichael L. Berumen
Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology (KAUST), Thuwal, 23955-6900 Saudi Arabia
Search for more papers by this authorLuiz A. Rocha
Section of Ichthyology, California Academy of Sciences, San Francisco, CA, 94118 USA
Search for more papers by this authorBrian W. Bowen
Hawai'i Institute of Marine Biology, University of Hawai'i, Kāne'ohe, HI, 96744 USA
Search for more papers by this authorCorresponding Author
Pauliina A. Ahti
Hawai'i Institute of Marine Biology, University of Hawai'i, Kāne'ohe, HI, 96744 USA
School of Life Sciences, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, G12 8QQ UK
Correspondence: Pauliina A. Ahti, School of Life Sciences, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow G12 8QQ, UK.
E-mail: [email protected]
Search for more papers by this authorRichard R. Coleman
Hawai'i Institute of Marine Biology, University of Hawai'i, Kāne'ohe, HI, 96744 USA
Search for more papers by this authorJoseph D. DiBattista
Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology (KAUST), Thuwal, 23955-6900 Saudi Arabia
Department of Environment and Agriculture, Curtin University, PO Box U1987, Perth, WA, 6845 Australia
Search for more papers by this authorMichael L. Berumen
Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology (KAUST), Thuwal, 23955-6900 Saudi Arabia
Search for more papers by this authorLuiz A. Rocha
Section of Ichthyology, California Academy of Sciences, San Francisco, CA, 94118 USA
Search for more papers by this authorBrian W. Bowen
Hawai'i Institute of Marine Biology, University of Hawai'i, Kāne'ohe, HI, 96744 USA
Search for more papers by this authorAbstract
Aim
The aim of this study was to resolve the evolutionary history, biogeographical barriers and population histories for sister species of wrasses, the African Coris (Coris cuvieri) in the Indian Ocean and Red Sea, and the Yellowtail Coris (Coris gaimard) in the Pacific Ocean. Glacial sea level fluctuations during the Pleistocene have shaped the evolutionary trajectories of Indo-Pacific marine fauna, primarily by creating barriers between the Red Sea, Indian Ocean and Pacific Ocean. Here, we evaluate the influence of these episodic glacial barriers on sister species C. cuvieri and C. gaimard.
Location
Red Sea, Indian Ocean, Pacific Ocean.
Methods
Sequences from mitochondrial DNA cytochrome oxidase c subunit I (COI), and nuclear introns gonadotropin-releasing hormone (GnRH) and ribosomal S7 protein were analysed in 426 individuals from across the range of both species. Median-joining networks, analysis of molecular variance and Bayesian estimates of the time since most recent common ancestor were used to resolve recent population history and connectivity.
Results
Cytochrome oxidase c subunit I haplotypes showed a divergence of 0.97% between species, and nuclear alleles were shared between species. No population structure was detected between the Indian Ocean and Red Sea. The strongest signal of population structure was in C. gaimard between the Hawaiian biogeographical province and other Pacific locations (COI ϕST = 0.040–0.173, P < 0.006; S7 ϕST = 0.046, P < 0.001; GnRH ϕST = 0.022, P < 0.005). Time to most recent common ancestor is c. 2.12 Ma for C. cuvieri and 1.76 Ma for C. gaimard.
Main conclusions
We demonstrate an Indian-Pacific divergence of < 2 Myr and high contemporary gene flow between the Red Sea and Indian Ocean, mediated in part by the long pelagic larval stage. The discovery of hybrids at Christmas Island indicates that Indian and Pacific lineages have come into secondary contact after allopatric isolation. Subspecies status may be appropriate for these two wrasses.
Supporting Information
Filename | Description |
---|---|
jbi12712-sup-0001-Suppinfo.docxWord document, 17.9 KB | Appendix S1 PCR reaction conditions and DNA fragment preparation. Appendix S2 Pairwise ϕST comparisons for Coris cuvieri. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Ahti, P.A. (2014) Phylogeography of Coris gaimard and Coris cuvieri in the Pacific Ocean, Indian Ocean, and Red Sea. MSci Thesis, University of Glasgow, Glasgow, UK.
- Andrews, K.R., Moriwake, V.N., Wilcox, C., Grau, E.G., Kelley, C., Pyle, R.L. & Bowen, B.W. (2014) Phylogeographic analyses of submesophotic snappers Etelis coruscans and Etelis “marshi” (Family Lutjanidae) reveal concordant genetic structure across the Hawaiian Archipelago. PLoS ONE, 9, e91665.
- Baldwin, C.C., Mounts, J.H., Smith, D.G. & Weight, L.A. (2009) Genetic identification and color descriptions of early life-history stages of Belizean Phaeoptyx and Astrapogon (Teleostei: Apogonidae) with comments on identification of adult Phaeoptyx. Zootaxa, 22, 1–22.
- Barber, P.H., Erdmann, M.V. & Palumbi, S.R. (2006) Comparative phylogeography of three codistributed stomatopods: origins and timing of regional lineage diversification in the Coral Triangle. Evolution, 60, 1825–1839.
- Bay, L.K., Choat, J.H., van Herwerden, L. & Robertson, D.R. (2004) High genetic diversities and complex genetic structure in an Indo-Pacific tropical reef fish (Chlorurus sordidus): evidence of an unstable evolutionary past? Marine Biology, 144, 757–767.
- Benjamini, Y. & Hochberg, Y. (2009) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B (Methodological), 57, 289–300.
- Bird, C.E., Holland, B.S., Bowen, B.W. & Toonen, R.J. (2011) Diversification of endemic sympatric limpets (Cellana spp.) in the Hawaiian Archipelago. Molecular Ecology, 20, 2128–2141.
- Bowen, B.W., Rocha, L.A., Toonen, R.J., Karl, S.A., Craig, M.T., DiBattista, J.D., Eble, J.A., Gaither, M.R., Skillings, D. & Bird, C.E. (2013) The origins of tropical marine biodiversity. Trends in Ecology & Evolution, 28, 359–366.
- Briggs, J.C. & Bowen, B.W. (2012) A realignment of marine biogeographic provinces with particular reference to fish distributions. Journal of Biogeography, 39, 12–30.
- Briggs, J.C. & Bowen, B.W. (2013) Evolutionary patterns: Marine shelf habitat. Journal of Biogeography, 40, 1023–1035.
- Caley, M.J. & Schluter, D. (2003) Predators favour mimicry in a tropical reef fish. Proceedings of the Royal Society B: Biological Sciences, 270, 667–672.
- Chow, S. & Hazama, K. (1998) Universal PCR primers for S7 ribosomal protein gene introns in fish. Molecular Ecology, 7, 1255–1256.
- Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772.
- DiBattista, J.D., Wilcox, C., Craig, M.T., Rocha, L.A. & Bowen, B.W. (2011) Phylogeography of the Pacific blueline surgeonfish, Acanthurus nigroris, reveals high genetic connectivity and a cryptic endemic species in the Hawaiian Archipelago. Journal of Marine Biology, 2011, Article ID 839134.
10.1155/2011/839134 Google Scholar
- DiBattista, J.D., Rocha, L.A., Craig, M.T., Feldheim, K.A. & Bowen, B.W. (2012) Phylogeography of two closely related Indo-Pacific butterflyfishes reveals divergent evolutionary histories and discordant results from mtDNA and microsatellites. Journal of Heredity, 103, 617–629.
- DiBattista, J.D., Roberts, M.B., Bouwmeester, J., Bowen, B.W., Coker, D.J., Lozano-Corté, J.F., Choat, J.H., Gaither, M.R., Hobbs, J-P.A., Khalil, M.T., Kochzius, M., Myers, R.F., Paulay, G., Robitzch, V.S.N., Saenz-Agudelo, P., Salas, E., Sinclair-Taylor, T.H., Toonen, R.J., Westneat, M.W., Williams, S.T. & Berumen, M.L. (In press) A review of contemporary patterns of endemism for shallow water reef fauna in the Red Sea. Journal of Biogeography. Online early.
- Drummond, A.J. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.
- Eble, J.A., Rocha, L.A., Craig, M.T. & Bowen, B.W. (2011) Not all larvae stay close to home: insights into marine population connectivity with a focus on the Brown Surgeonfish (Acanthurus nigrofuscus). Journal of Marine Biology, 2011, Article ID 518516.
10.1155/2011/518516 Google Scholar
- Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47–50.
- Faurby, S. & Barber, P.H. (2012) Theoretical limits to the correlation between pelagic larval duration and population genetic structure. Molecular Ecology, 21, 3419–3432.
- Fernandez-Silva, I., Randall, J.E., Coleman, R.R., DiBattista, J.D., Rocha, L.A., Reimer, J.D., Meyer, C.G. & Bowen, B.W. (2015) Yellow tails in a Red Sea: phylogeography of the Indo-Pacific goatfish Mulloidichthys flavolineatus reveals isolation in peripheral provinces and cryptic evolutionary lineages. Journal of Biogeography, 42, 2402–2413.
- Ferry-Graham, L.A., Wainright, P.C., Westneat, M.W. & Bellwood, D.R. (2002) Mechanisms of benthic prey capture in wrasses (Labridae). Marine Biology, 141, 819–830.
- Fruciano, C., Hanel, R., Debes, P.V., Tigano, C. & Ferrito, V. (2011) Atlantic-Mediterranean and within-Mediterranean molecular variation in Coris julis (L. 1758) (Teleostei, Labridae). Marine Biology, 158, 1271–1286.
- Fu, Y.-X. (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147, 915–925.
- Gaither, M.R. & Rocha, L.A. (2013) Origins of species richness in the Indo-Malay-Philippine biodiversity hotspot: evidence for the centre of overlap hypothesis. Journal of Biogeography, 40, 1638–1648.
- Gaither, M.R., Bowen, B.W., Bordenave, T.-R., Rocha, L.A., Newman, S.J., Gomez, J.A., van Herwerden, L. & Craig, M.T. (2011) Phylogeography of the reef fish Cephalopholis argus (Epinephelidae) indicates Pleistocene isolation across the Indo-Pacific barrier with contemporary overlap in the coral triangle. Evolutionary Biology, 189, 1–15.
- Grant, W.S. & Bowen, B.W. (1998) Shallow population histories in deep evolutionary lineages of marine fishes: Insights from sardines and anchovies and lessons for conservation. The Journal of Heredity, 89, 415–426.
- Guillemaud, T., Cancela, M.L., Afonso, P., Morato, T., Santos, R.S. & Wirtz, P. (2000) Molecular insights into the taxonomic status of Coris atlantica (Pisces: Labridae). Journal of the Marine Biological Association of the UK, 80, 929–933.
- Guindon, S. & Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704.
- Harper, G.R. & Pfennig, D.W. (2008) Selection overrides gene flow to break down maladaptive mimicry. Nature, 451, 1103–1106.
- Hassan, M., Lemaire, C., Fauvelot, C. & Bonhomme, F. (2002) Seventeen new exon-primed intron-crossing polymerase chain reaction amplifiable introns in fish. Molecular Ecology Notes, 2, 334–340.
- Hobbs, J.-P.A. & Allen, G.R. (2014) Hybridisation among coral reef fishes at Christmas Island and the Cocos (Keeling) Islands. Raffles Bulletin of Zoology, 30, 220–226.
- Hobbs, J.-P.A., Frisch, A.J., Allen, G.R. & van Herwerden, L. (2009) Marine hybrid hotspot at Indo-Pacific biogeographic border. Biology Letters, 5, 258–261.
- Hobbs, J.-P.A., Newman, S.J., Mitsopoulos, G.E.A., Travers, M.J., Skepper, C.L., Gilligan, J.J., Allen, G.R., Choat, H.J. & Ayling, A.M. (2014) Checklist and new records of Christmas Island fishes: the influence of isolation, biogeography and habitat availability on species abundance and community composition. Raffles Bulletin of Zoology, 30, 182–202.
- Hourigan, T.F. & Reese, E.S. (1987) Mid-ocean isolation and the evolution of Hawaiian reef fishes. Trends in Ecology and Evolution, 2, 187–191.
- Johns, G.C. & Avise, J.C. (1998) A comparative summary of genetic distances in the vertebrates from the mitochondrial cytochrome b gene. Molecular Biology and Evolution, 15, 1481–1490.
- Keith, S.A., Woolsey, P.S., Madin, J.S., Byrne, M. & Baird, A. (2015) Differential establishment potential of species predicts a shift in coral assemblage structure across a biogeographic barrier. Ecography, 38, 1–10.
- Kemp, J. (1998) Zoogeography of the coral reef fishes of the Socotra Archipelago. Journal of Biogeography, 25, 919–933.
- Klausewitz, W. (1989) Evolutionary history and zoogeography of the Red Sea ichtyofauna. Fauna of Saudi Arabia, 10, 310–337.
- Kobayashi, D.R. (2006) Colonization of the Hawaiian Archipelago via Johnston Atoll: a characterization of oceanographic transport corridors for pelagic larvae using computer simulation. Coral Reefs, 25, 407–417.
- Leray, M., Beldade, R., Holbrook, S.J., Scmitt, R.J., Planes, S. & Bernardi, G. (2010) Allopatric divergence and speciation in coral reef fish: the three-spot dascyllus, Dascyllus trimaculatus, species complex. Evolution, 64, 1218–1230.
- Librado, P. & Rozas, J. (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.
- Liu, S.-Y.V., Chang, F.-T., Borsa, P., Chen, W.-J. & Dai, C.-F. (2014) Phylogeography of the humbug damselfish, Dascyllus aruanus (Linnaeus, 1758): evidence of Indo-Pacific vicariance and genetic differentiation in peripheral populations. Biological Journal of the Linnean Society, 113, 931–942.
- Ludt, W.B. & Rocha, L.A. (2015) Shifting seas: the impacts of Pleistocene sea-level fluctuations on the evolution of tropical marine taxa. Journal of Biogeography, 42, 25–38.
- Ludt, W.B., Bernal, M.A., Bowen, B.W. & Rocha, L.A. (2012) Living in the past: phylogeography and population histories of Indo-Pacific wrasses (genus Halichoeres) in shallow lagoons versus outer reef slopes. PLoS ONE, 7, e38042.
- McMillan, W.O., Weigt, L.A. & Palumbi, S.R. (1999) Color pattern evolution, assortative mating, and genetic differentiation in brightly colored butterflyfishes (Chaetodontidae). Evolution, 53, 247–260.
- Meeker, N.D., Hutchinson, S.A., Ho, L. & Trede, N.S. (2007) Method for isolation of PCR-ready genomic DNA from zebrafish tissues. BioTechniques, 43, 610–614.
- Montanari, S.R., Hobbs, J.-P.A., Pratchett, M.S., Bay, L.K. & van Herwerden, L. (2014) Does genetic distance between parental species influence outcomes of hybridization among coral reef butterflyfishes? Molecular Ecology, 11, 2757–2770.
- New, A.L., Alderson, S.G., Smeed, D.A. & Stansfield, K.L. (2007) On the circulation of water masses across the Mascarene Plateau in the South Indian Ocean. Deep-Sea Research, 54, 42–74.
- Obura, D. (2012) The diversity and biogeography of Western Indian Ocean reef-building corals. PLoS ONE, 7, e45013.
- Peakall, R. & Smouse, P.E. (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6, 288–295.
- Peakall, R. & Smouse, P.E. (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research–an update. Bioinformatics, 28, 2537–2539.
- Pfennig, D.W., Harcombe, W.R. & Pfennig, K.S. (2001) Frequency-dependent Batesian mimicry. Nature, 410, 323.
- Randall, J.E. (1998) Zoogeography of shore fishes of the Indo-Pacific region. Zoological Studies, 37, 227–268.
- Randall, J.E. (1999) Revision of the Indo-Pacific fishes of the genus Coris, with descriptions of five new species. Indo-Pacific Fishes, 29, 1–74.
- Randall, J.E. (2005) A review of mimicry in marine fishes. Zoological Studies, 44, 299–328.
- Randall, J.E. (2007) Reef and shore fishes of the Hawaiian Islands. University of Hawaii Sea Grant Program, Honolulu, HI.
- Reece, J.S., Bowen, B.W., Smith, D. & Larson, A. (2011) Comparative phylogeography of four Indo-Pacific moray eel species (Muraenidae) reveals comparable ocean-wide genetic connectivity despite five-fold differences in available adult habitat. Marine Ecology Progress Series, 437, 269–277.
- Reininger, M. (2011) Mimicry in juvenile wrasses: ecological and behavioural aspects of a Coris-Amphiprion relationship in the northern Red Sea. Zoology in the Middle East, 54, 23–34.
- Roberts, C.M., Shepherd, A.R.D. & Ormond, R.F.G. (1992) Large-scale variation in assemblage structure of Red Sea butterflyfishes and angelfishes. Journal of Biogeography, 19, 239–250.
- Rocha, L.A. (2004) Mitochondrial DNA and color pattern variation in three western Atlantic Halichoeres (Labridae), with the revalidation of two species. Copeia, 2004, 770–782.
- Rocha, L.A., Bass, A.L., Robertson, D.R. & Bowen, B.W. (2002) Adult habitat preferences, larval dispersal, and the comparative phylogeography of three Atlantic surgeonfishes (Teleostei: Acanthuridae). Molecular Ecology, 11, 243–252.
- Sale, P.F. (1980) The ecology of fishes on coral reefs. Oceanography and Marine Biology, 18, 367–421.
- Selkoe, K.A., Gaggiotti, O.E., ToBo Laboratory, Bowen, B.W. & Toonen, R.J. (2014) Emergent patterns of population genetic structure for a coral reef community. Molecular Ecology, 23, 3064–3079.
- Siddal, M., Rohling, E.J., Almongi-Labin, A., Hemleben, C., Meischner, D., Scmelzer, I. & Smeed, D.A. (2003) Sea-level fluctuations during the last glacial cycle. Nature, 423, 853–858.
- Stephens, M. & Donnelly, P. (2003) A comparison of Bayesian methods for haplotype reconstruction from population genotype data. American Journal of Human Genetics, 73, 1162–1169.
- Tamura, K. & Nei, M. (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10, 512–526.
- Timm, J. & Kochzius, M. (2008) Geological history and oceanography of the Indo-Malay Archipelago shape the genetic population structure in the false clown anemonefish (Amphiprion ocellaris). Molecular Ecology, 17, 3999–4014.
- Toonen, R.J., Andrews, K.R., Baums, I.B., Bird, C.E., Concepcion, G.T., Daly-Engel, T.S., Eble, J.A., Faucci, A., Gaither, M.R., Iacchei, M., Puritz, J.B., Schultz, J.K., Skillings, D.J., Timmers, M.A. & Bowen, B.W. (2011) Defining boundaries for ecosystem-based management: a multispecies case study of marine connectivity across the Hawaiian Archipelago. Journal of Marine Biology, 2011, Article ID 460173.
- Victor, B.C. (1986) Duration of the planktonic larval stage of one hundred species of Pacific and Atlantic wrasses (family Labridae). Marine Biology, 90, 317–326.
- Ward, R.D., Zemlak, T.S., Innes, B.H., Last, P.R. & Hebert, P.D.N. (2005) DNA barcoding Australia's fish species. Philosophical Transactions of the Royal Society B: Biological sciences, 360, 1847–1857.