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Hybridization of reef fishes at the Indo-Pacific biogeographic barrier: a case study

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Abstract

Hybridization is recognized as an important source of genetic variation. In some reef fishes, including the Acanthuridae, hybridization has been detected due to intermediate colouration. This study used a molecular genetic approach to investigate hybridization in two Acanthurid species: Acanthurus leucosternon and Acanthurus nigricans, which have Indian and Pacific Ocean distributions respectively and are sympatric in the eastern Indian Ocean. In this area a putatitve hybrid, Acanthurus cf. leucosternon has been recognized based on intermediate colouration and restriction to the sympatric region of otherwise allopatric putative parental species. This study aimed to test this hypothesis using genetic tools. The three species were sampled from Cocos (Keeling) and Christmas Islands, the biogeographic boundary where many Indian and Pacific Ocean biota meet. Representatives from allopatric populations of both parental species and outgroups were also sampled. Mitochondrial COI and intron 1 of the nuclear ribosomal protein S7 were sequenced from 13 and 30 specimens respectively. Although sample sizes in this study are relatively small and more genetic data, including an extended phylogeographic sampling, is required to further evaluate these findings, the COI results support hybrid origins of Acanthurus cf. leucosternon, but S7 data are inconclusive due to the possibility of incomplete lineage sorting. The fourfold more abundant Acanthurus nigricans is most often the maternal parent. Inter-fertile hybrids apparently backcross with rare Acanthurus leucosternon males, transferring Acanthurus nigricans mitochondria to this species. These results suggest that Acanthurus leucosternon may eventually be lost from these islands, due to their relative rarity and introgressive hybridization.

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References

  • Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, New York

    Google Scholar 

  • Arnold ML, Hodges SA (1995) Are natural hybrids fit or unfit relative to their parents? Trends Ecol Evol 10:67–71

    Article  Google Scholar 

  • Barton NH (2001) The role of hybridization in evolution. Mol Ecol 10:551–568

    Article  PubMed  CAS  Google Scholar 

  • Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Annu Rev Ecol Syst 16:113–148

    Article  Google Scholar 

  • Bernardi G, Holbrook SJ, Schmitt RJ (2001) Gene flow at three spatial scales in a coral reef fish, the three-spot dascyllus, Dascyllus trimaculatus. Mar Biol 138:457–465

    Article  CAS  Google Scholar 

  • Bernardi G, Holbrook SJ, Schmitt RJ, Crane NL, DeMartini E (2002) Species boundaries, populations and colour morphs in the coral reef three-spot damselfish (Dascyllus trimaculatus) species complex. Proc R Soc B Biol Sci 269:599–605

    Article  Google Scholar 

  • Bernardi G, Bucciarelli G, Costagliola D, Robertson DR, Heiser JB (2004) Evolution of coral reef fish Thalassoma spp. (Labridae). 1. Molecular phylogeny and biogeography. Mar Biol 144:369–375

    Article  Google Scholar 

  • Brown LD (1995) Genetic evidence for hybridization between Haliotis rubra and H. laevigata. Mar Biol 123:89–93

    Article  CAS  Google Scholar 

  • Chow S, Hazama K (1998) Universal PCR primers for S7 ribosomal protein gene introns in fish. Mol Ecol 7:1255–1256

    PubMed  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinformatics Online 1:47–50

    CAS  Google Scholar 

  • Folmer O, Black M, Hoen W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    PubMed  CAS  Google Scholar 

  • Frisch A, van Herwerden L (2006) Field and experimental studies of hybridization between coral trouts, Plectropomus leopardus and Plectropomus maculatus (Serranidae), on the Great Barrier Reef, Australia. J Fish Biol 68:1013–1025

    Article  Google Scholar 

  • Garcia-Machado E, Chevalier Monteagudo P, Solignac M (2004) Lack of mtDNA differentiation among hamlets (Hypoplectrus, Serranidae). Mar Biol 144:147–152

    Article  CAS  Google Scholar 

  • Gardner JPA (1996) The Mytilus edulis species complex in southwest England: effects of hybridization and introgression upon interlocus associations and morphometric variation. Mar Biol 125:385–399

    Article  Google Scholar 

  • Grant PR, Grant BR, Petren K (2005) Hybridization in the recent past. Am Nat 166:56–67

    Article  PubMed  Google Scholar 

  • Hall TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Harrison RG (1993) Hybrid zones and the evolutionary process. Oxford University Press, Oxford

    Google Scholar 

  • Hutchinson WF, Carvalho GR, Rogers SI (2001) Marked genetic structuring in localised spawning populations of cod (Gadus morhua) within the North Sea and adjoining waters as revealed by microsatellites. Mar Ecol Prog Ser 223:251–260

    Article  Google Scholar 

  • Jansson H, Holmgren I, Wedin K, Andersson T (1991) High frequency of natural hybrids between Atlantic salmon, Salmo salar L., and brown trout, S. truta L., in a Swedish river. J Fish Biol 39:343–348

    Article  Google Scholar 

  • Klanten S, van Herwerden L, Choat JH, Blair D (2004) Patterns of lineage diversification in the genus Naso (Acanthuridae). Mol Phylogenet Evol 32:221–235

    Article  PubMed  CAS  Google Scholar 

  • Knowlton N (2000) Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 420:73–90

    Article  CAS  Google Scholar 

  • Kuiter RH, Debelius H (2001) Surgeonfishes, rabbitfishes and their relatives. A comprehensive guide to Acanthuroidei (marine fish families). TMC Publishing, Chorleywood

    Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analyses and sequence alignment. Briefings in Bioinformatics 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Lacson JM (1994) Fixed allele frequency differences among Palauan and Okinawan populations of the damselfishes Chrysiptera cyanea and Pomacentrus coelestis. Mar Biol 118:359–365

    Article  CAS  Google Scholar 

  • Lacson JM Clark S (1995) Genetic divergence of Maldivian and Micronesian demes of the damselfishes Stegastes nigricans, Crysiptera biocellata, C. glauca and C. leucopoma (Pomacentridae). Mar Biol 121:585–590

    Article  Google Scholar 

  • Lacson JM, Nelson SG (1993) Genetic distances among fishes of the genus Siganus (Siganidae) from the western Pacific Ocean. Mar Biol 116:187–192

    Article  CAS  Google Scholar 

  • Lessios HA, Kessing BD, Robertson DR, Paulay G (1999) Phylogeography of the pantropical sea urchin Eucidaris in relation to land barriers and ocean currents. Evolution 53:806–817

    Article  Google Scholar 

  • Lieske E, Meyers R (1999) Coral reef fishes. Princeton University Press, Princeton

    Google Scholar 

  • Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20:229–237

    Article  PubMed  Google Scholar 

  • McCartney MA, Acevedo J, Heredia C, Rico C, Quenoville B, Bermingham E, McMillan O (2003) Genetic mosaic in a marine species flock. Mol Ecol 12:2963–2973

    Article  PubMed  CAS  Google Scholar 

  • McMillan WO, Weight LA, Palumbi SR (1999) Color pattern evolution, assortative mating, and genetic differentiation in brightly colored butterflyfishes (Chaetodontidae). Evolution 53:247–260

    Article  Google Scholar 

  • Messmer V, van Herwerden L, Munday P, Jones GP (2005) Phylogeography of colour polymorphism in the coral reef fish Pseudochromis fuscus, from Papua New Guinea and the Great Barrier Reef. Coral Reefs 24:392–402

    Article  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Planes S, Doherty P (1997) Genetic and color interactions at a contact zone of Acanthochromis polyacanthus—a marine fish lacking pelagic larvae. Evolution 51:1232–1243

    Article  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Ramon ML, Lobel S, Sorenson MD (2003) Lack of mitochondrial genetic structure in hamlets (Hypoplectrus spp.); recent speciation or ongoing hybridization. Mol Ecol 12:2975–2980

    Article  PubMed  Google Scholar 

  • Read C, Bellwood D, van Herwerden L (2006) Ancient origins of Indo-Pacific coral reef fish biodiversity: a case study of the leopard wrasses (Labridae: Macropharyngodon). Mol Phylogenet Evol 38:808–819

    Article  PubMed  CAS  Google Scholar 

  • Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109

    Article  Google Scholar 

  • Ruzzante DE, Taggart CT, Lang S, Cook D (2000) Mixed-stock analysis of Atlantic cod near the Gulf of St Lawrence based on microsatellite DNA. Ecol Appl 10:1090–1109

    Article  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Swofford DL (1999) PAUP*: phylogenetic analysis using parsimony. Sinauer Associates, Champaign

    Google Scholar 

  • Taylor EB, Boughman JW, Groenenboom M, Sniatynski M, Schluter D, Gow JL (2006) Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair. Mol Ecol 15:343–356

    Article  PubMed  CAS  Google Scholar 

  • Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Carribbean reef fish. Science 299:107–109

    Article  PubMed  CAS  Google Scholar 

  • van Herwerden L, Doherty P (2006) Contrasting genetic structures across two hybrid zones of a tropical reef fish, I (Bleeker 1855). J Evol Biol 19:239–252

    Article  PubMed  Google Scholar 

  • van Herwerden L, Choat JH, Dudgeon CL, Carlos G, Newman SJ, Frisch A, van Oppen M (2006) Contrasting patterns of genetic structure in two species of the coral trout Plectropomus (Serranidae) from east and west Australia: introgressive hybridization or ancestral polymorphisms. Mol Phylogenet Evol 41:420–435

    Article  PubMed  Google Scholar 

  • van Oppen MJH, Gates RD (2006) Conservation genetics and the resilience of reef-building corals. Mol Ecol 15:3863–3883

    Article  PubMed  Google Scholar 

  • Wilkins NP, Courtney HP, Gosling E, Linnane A, Jordan C, Curatolo A (1994) Morphometric and meristic characters in salmon, Salmo salar L., trout, Salmo truta L., and their hybrids. Aquaculture and Fisheries Management 25:505–518

    Google Scholar 

  • Williams` ST, Benzie JAH (1998) Evidence of a biogeographic break between populations of a high dispersal starfish: congruent regions within the Indo-West Pacific defined by color morphs, mtDNA, and allozyme data. Evolution 52:87–99

    Article  Google Scholar 

  • Yaakub SM, Bellwood DR, van Herwerden L, Walsh FM (2006) Hybridization in coral reef fishes: introgression and bi-directional gene exchange in Thalassoma (family Labridae). Mol Phylogenet Evol 40:84–100

    Article  PubMed  CAS  Google Scholar 

  • Yaakub SM, Bellwood DR, van Herwerden L (2007) A rare hybridization event in two common Caribbean wrasses (genus Halichoeres; family Labridae). Coral Reefs. doi: 10.1007/s00338-007-0240-z

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Acknowledgements

Our thanks to: Justin Gilligan, Jay Hender and Dr Robertson, who provided field assistance and helped in collecting the specimens. Thanks also to Parks Australia Christmas Island, John Clunies-Ross and Geof Christie for providing valuable logistical support. We also thank Selma Klanten for guidance in the laboratory and COI sequences for the outgroups. Thanks are further due to Claire Farnsworth and Kate Winters for assistance with labwork. This work was funded by James Cook University funds awarded to JH Choat, GP Jones, P Munday and D Jerry.

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Authors and Affiliations

  1. Molecular Ecology and Evolution Laboratory, James Cook University, Townsville, QLD, 4811, Australia

    A. D. Marie, L. van Herwerden, J. H. Choat & J-P. A. Hobbs

  2. Discipline Marine Biology and Aquaculture, School of Marine and Tropical Biology, James Cook University, Townsville, QLD, 4811, Australia

    L. van Herwerden

  3. ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD, 4811, Australia

    J-P. A. Hobbs

  4. Department of Biology, University of Sherbrooke, Sherbrooke, QC, Canada, J1K 2W5

    A. D. Marie

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  1. A. D. Marie
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  2. L. van Herwerden
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  3. J. H. Choat
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  4. J-P. A. Hobbs
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Correspondence to L. van Herwerden.

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Communicated by Biology Editor M. van Oppen.

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Marie, A.D., van Herwerden, L., Choat, J.H. et al. Hybridization of reef fishes at the Indo-Pacific biogeographic barrier: a case study. Coral Reefs 26, 841–850 (2007). https://doi.org/10.1007/s00338-007-0273-3

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  • DOI: https://doi.org/10.1007/s00338-007-0273-3

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