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Extreme genetic diversity and temporal rather than spatial partitioning in a widely distributed coral reef fish

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Abstract

Mitochondrial control region (HVR-1) sequences were used to identify patterns of genetic structure and diversity in Naso vlamingii, a widespread coral reef fish with a long evolutionary history. We examined 113 individuals from eight locations across the Indo-Pacific Ocean. Our aims were to determine the spatial scale at which population partitioning occurred and then to evaluate the extent to which either vicariance and/or dispersal events have shaped the population structure of N. vlamingii. The analysis produced several unexpected findings. Firstly, the genetic structure of this species was temporal rather than spatial. Secondly, there was no evidence of a barrier to dispersal throughout the vast distribution range. Apparently larvae of this species traverse vicariance barriers that inhibit inter-oceanic migration of other widespread reef fish taxa. Thirdly, an unusual life history and long evolutionary history was associated with a population structure that was unique amongst coral reef fishes in terms of the magnitude and pattern of genetic diversity (haplotype diversity, = 1.0 and nucleotide diversity π = 13.6%). In addition to these unique characteristics, there was no evidence of isolation by distance (= 0.458, R 2 = 0.210, = 0.078) as has also been shown for some other widespread reef species. However, some reductions in gene flow were observed among and within Ocean basins [Indian–Pacific analysis of molecular variance (AMOVA), Φ st = 0.0766, < 0.05; West Indian–East Indian–Pacific AMOVA Φ st = 0.079, < 0.05]. These findings are contrasted with recent studies of coral reef fishes that imply a greater degree of spatial structuring in coral reef fish populations than would be expected from the dispersive nature of their life cycles. We conclude that increased taxon sampling of coral reef fishes for phylogeographic analysis will provide an extended view of the ecological and evolutionary processes shaping coral reef fish diversity at both ends of the life history spectrum.

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References

  • Abesamis RA, Russ GR (2005) Density-dependent spillover from a marine reserve: long-term evidence. Ecol Appl 15:1798–1812

    Google Scholar 

  • Alvarado Bremer JR, Baker AJ, Mejuto J (1995) Mitochondrial DNA control region sequences indicate extensive mixing of swordfish (Xiphias gladius) populations in the Atlantic Ocean. Can J Fish Aquat Sci 52:1720–1732

    Article  Google Scholar 

  • Alvarado Bremer JR, Vinas J, Mejuto J, Ely B, Pla C (2005) Comparative phylogeography of Atlantic bluefin tuna and swordfish: the combined effects of vicariance, secondary contact, introgression, and population expansion on the regional phylogenies of two highly migratory pelagic fishes. Mol Phylogenet Evol 36:169–187

    Article  PubMed  CAS  Google Scholar 

  • Avise JC (1998) Conservation genetics in the marine realm. J Hered 89:377–382

    Article  Google Scholar 

  • Barber PH, Palumbi SR, Erdmann MV, Moosa MK (2000) A marine Wallace’s line? Nature 406:692–693

    Article  PubMed  CAS  Google Scholar 

  • Barber PH, Moosa MK, Palumbi SR (2002) Rapid recovery of genetic populations on Krakatau: diversity of stomatopod temporal and spatial scales of marine larval dispersal. Proc R Soc Lond B 269:1591–1597

    Article  CAS  Google Scholar 

  • Bay LK, Choat JH, van Herwerden L, Robertson DR (2004) High genetic diversities and complex genetic structure in an Indo-Pacific tropical reef fish (Chlorurus sordidus): evidence of an unstable evolutionary past? Mar Biol 144:757–767

    Article  CAS  Google Scholar 

  • Berkeley SA, Chapman C, Sogard SM (2004) Maternal age as a determinant of larval growth and survival in a marine fish, Sebastes melanops. Ecology 85:1258–1264

    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 

  • Bohonak AJ (2002) IBD (isolation by distance): a program for analyses of isolation by distance. J Hered 93:153–154

    Article  PubMed  CAS  Google Scholar 

  • Bowen BW, Bass AL, Rocha LA, Grant WS, Robertson DR (2001) Phylogeography of the trumpetfishes (Aulostomus): ring species complex on a global scale. Evolution 55:1029–1039

    Article  PubMed  CAS  Google Scholar 

  • Bowen BW, Muss A, Rocha LA, Grant WS (2006) Shallow mtDNA coalescence in atlantic pygmy angelfishes (genus Centropyge) indicates a recent invasion from the Indian Ocean. J Hered 97:1–12

    Article  PubMed  CAS  Google Scholar 

  • Choat JH, Clements KD (1998) Vertebrate herbivory in marine and terrestrial environments: a nutritional ecology perspective. Annu Rev Ecol Syst 29:375–403

    Article  Google Scholar 

  • Choat JH, Robertson DR (2002) Age-based studies. In: Sale PF (ed) Coral reef fishes, dynamics and diversity in a complex ecosystem. Academic, San Diego, pp. 57–80

    Google Scholar 

  • Choat JH, Clements KD, Robbins WD (2002) The trophic status of herbivorous fishes on coral reefs. I: dietary analyses. Mar Biol 140:613–623

    Article  CAS  Google Scholar 

  • Choat JH, Robbins WD, Clements KD (2004) The trophic status of herbivorous fishes on coral reefs. Mar Biol 145:445–454

    Article  Google Scholar 

  • Cuvier G, Valenciennes MA (1835) Histoire naturelle des poissons. Réimpression 1969, vol X. Asher, Amsterdam, pp 482

  • Doherty PJ, Mather P, Planes S (1994) Acanthochromis polyacanthus, a fish lacking larval dispersal, has genetically differentiated populations at local and regional scales on the Great Barrier Reef. Mar Biol 121:11–21

    Article  Google Scholar 

  • Duda TF, Kohn AJ (2005) Species-level phylogeography and evolutionary history of the hyperdiverse marine gastropod genus Conus. Mol Phylogenet Evol 34:257–272

    Article  PubMed  Google Scholar 

  • Ely B, Viñas J, Alvarado Bremer JR, Black D, Lucas L, Covello K, Labrie AV, Thelen E (2005) Consequences of the historical demography on the global population structure of two highly migratory cosmopolitan marine fishes: the yellowfin tuna (Thunnus albacares) and the skipjack tuna (Katsuwonus pelamis). BMC Evol Biol 5:9

    Article  Google Scholar 

  • Excoffier L (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Mol Ecol 13:853–864

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed  CAS  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    PubMed  CAS  Google Scholar 

  • Hallam A (1984) Pre-Quaternary sea-level changes. Annu Rev Earth Planet Sci 12:205–243

    Article  CAS  Google Scholar 

  • Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600

    PubMed  CAS  Google Scholar 

  • Harpending HC, Batzer MA, Gurven M, Jorde LB, Rogers AR, Sherry ST (1998) Genetic traces of ancient demography. Proc Natl Acad Sci USA 95:1961–1967

    Article  PubMed  CAS  Google Scholar 

  • Helfman GS, Colette BB, Facey DE (1997) The diversity of fishes. Blackwell Science, Massachusetts

    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 coral trout Plectropomus (Serranidae) from east and west Australia: introgressive hybridisation or ancestral polymorphisms. Mol Phylogenet Evol (in press)

  • Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276

    Article  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MR. BAYES: bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Jones GP, Milicich MJ, Emslie JJ, Lunow C (1999) Self-recruitment in a coral reef fish population. Nature 402:802–804

    Article  CAS  Google Scholar 

  • Kinlan BP, Gaines SD (2003) Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84:2007–2020

    Google Scholar 

  • Kinlan BP, Gaines SD, Lester SE (2005) Propagule dispersal and the scales of marine community process. Divers Distrib 11:139–148

    Article  Google Scholar 

  • Klanten SO, 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 

  • Kuiter RH, Debelius H (2001) Surgeonfishes, rabbitfishes and their relatives. TMC Publishing, Chorleywood

    Google Scholar 

  • Leis JM, Carson-Ewart BM (1997) In situ swimming speeds of the late pelagic larvae of some Indo-Pacific coral-reef fishes. Mar Ecol Prog Ser 159:165–174

    Google Scholar 

  • Leis JM, McCormick MI (2002) The biology, behavior, and ecology of the pelagic, larval stage of coral reef fishes. In: Sale PF (ed) Coral reef fishes, dynamics and diversity in a complex ecosystem. Academic, San Diego, pp. 171–199

    Google Scholar 

  • Leis JM, Richards WJ (1984) Acanthuroidei: development and relationships. Am. Soc. Ichthyologists & Herpetologists, La Jolla

  • Lessios HA, Kessing BD, Robertson DR (1998) Massive gene flow across the world’s most potent marine biogeographic barrier. Proc R Soc Lond B 265:583–588

    Article  Google Scholar 

  • Lessios HA, Kessing BD, Pearse JS (2001) Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema. Evolution 55:955–975

    Article  PubMed  CAS  Google Scholar 

  • Lessios HA, Kane J, Robertson DR (2003) Phylogeography of the pantropical sea urchin Tripneustes: contrasting patterns of population structure between oceans. Evolution 57:2026–2036

    Article  PubMed  CAS  Google Scholar 

  • Li WH (1977) Distribution of nucleotide differences between two randomly chosen cistrons in a finite population. Genetics 85:331–337

    PubMed  CAS  Google Scholar 

  • McMillan WO, Palumbi SR (1997) Rapid rate of control-region evolution in Pacific Butterflyfishes (Chaetodontidae). J Mol Evol 45:473–484

    Article  PubMed  CAS  Google Scholar 

  • Messmer V, van Herwerden L, Munday P, Jones G (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 

  • Meyer CP, Geller JB, Paulay G (2005) Fine scale endemism on coral reefs: Archipelagic differentiation in turbinid gastropods. Evolution 59:113–125

    Article  PubMed  Google Scholar 

  • Miller KG, Kominz MA, Browning JV, Wright JD, Mountain GS, Katz ME, Sugarman PJ, Cramer BS, Christie-Blick N, Pekar SF (2005) The phanerozoic record of global sea-level change. Science 310:1293–1298

    Article  PubMed  CAS  Google Scholar 

  • Munday PL, van Herwerden L, Dudgeon CL (2004) Evidence for sympatric speciation by host shift in the sea. Curr Biol 14:1498–1504

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Nichols RA, Hewitt GM (1994) The genetic consequences of long-distance dispersal during colonization. Heredity 72:312–317

    Google Scholar 

  • Palumbi SR (1992) Marine speciation on a small planet. Trends Ecol Evol 7:114–118

    Article  Google Scholar 

  • Palumbi SR (1997) Molecular biogeography of the Pacific. Coral Reefs 16(Suppl.):S47–S52

    Article  Google Scholar 

  • Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:S146–S158

    Google Scholar 

  • Palumbi SR (2004) Marine reserves and ocean neighborhoods: the spatial scale of marine populations and their management. Annu Rev Environ Resour 29:31–68

    Article  Google Scholar 

  • Pears RJ, Choat JH, Mapstone BD, Begg GA (2006) Demography of a large grouper, Epinephelus fuscoguttatus, from Australia’s Great Barrier Reef: implications for fishery management. Mar Ecol Prog Ser 307:259–272

    Google Scholar 

  • Pianka ER (1978) Evolutionary ecology. Harper & Row Publishers, New York

    Google Scholar 

  • Pickering KT (2000) The Cenozoic world. In: Culver SJ, Rawson PF (eds) Biotic response to global change. Cambridge University Press, Cambridge, pp. 20–34

    Google Scholar 

  • Planes S, Fauvelot C (2002) Isolation by distance and vicariance drive genetic structure of a coral reef fish in the Pacific Ocean. Evolution 56:378–399

    Article  PubMed  CAS  Google Scholar 

  • Planes S, Doherty PJ, Bernardi G (2001) Strong genetic divergence among populations of a marine fish with limited dispersal, Acanthochromis polyacanthus, within the Great Barrier Reef and the Coral Sea. Evolution 55:2263–2273

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • de Queiroz A (2005) The resurrection of oceanic dispersal in historical biogeography. Trends Ecol Evol 20:68–73

    Article  PubMed  Google Scholar 

  • Rambaut A (1996) Se-Al: sequence alignment editor. http://evolve.zoo.ox.ac.uk

  • Randall JE (2002) Surgeonfishes of Hawai’i and the world. Mutual Publishing & Bishop Museum Press, Honolulu

    Google Scholar 

  • Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol 20:76–86

    Article  PubMed  CAS  Google Scholar 

  • Read CI, Bellwood DR, 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 

  • Robertson DR (1982) Fish feces as fish food on a Pacific coral reef. Mar Ecol Prog Ser 7:253–265

    Google Scholar 

  • Rocha LA, Bass AL, Robertson DR, Bowen BW (2002) Adult habitat preferences, larval dispersal, and the comparative phylogeography of three Atlantic surgeonfishes (Teleostei: Acanthuridae). Mol Ecol 11:243–252

    Article  PubMed  CAS  Google Scholar 

  • Rocha LA, Robertson DR, Roman J, Bowen BW (2005) Ecological speciation in tropical reef fishes. Proc R Soc Lond B 272:573–579

    Article  Google Scholar 

  • Rogers AR (1995) Genetic evidence for a Pleistocene population explosion. Evolution 49:608–615

    Article  Google Scholar 

  • Rogers AR, Harpending HC (1992) Population-growth makes waves in the distribution of pairwise genetic-differences. Mol Biol Evol 9:552–569

    PubMed  CAS  Google Scholar 

  • Sale PF (2002) Coral reef fishes, dynamics and diversity in a complex ecosystem. Academic, San Diego

    Google Scholar 

  • Sambrook J, Fritsh EF, Maniatis T (1989) Molecular cloning, a laboratory manual. Cold Spring Harbour Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Sanderson MJ (1997) A nonparametric approach to estimating divergence times in the absence of rate constancy. Mol Biol Evol 14:1218–1231

    CAS  Google Scholar 

  • Sanderson MJ (2003) r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19:301–302

    Article  PubMed  CAS  Google Scholar 

  • Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates very among sites: application to human mitochondrial DNA. Genetics 152:1079–1089

    PubMed  CAS  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) A software for population genetics data analysis (ARLEQUIN)

  • Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47:264–279

    Article  Google Scholar 

  • Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562

    PubMed  CAS  Google Scholar 

  • Stepien CA, Randall JE, Rosenblatt RH (1994) Genetic and morphological divergence of a circumtropical complex of goatfishes: Mulloidichthys vanicolensis, M. dentatus, and M. martinicus. Pac Sci 48:44–56

    Google Scholar 

  • Stobutzki IC (1997) Energetic cost of sustained swimming in the late pelagic stages of reef fishes. Mar Ecol Prog Ser 152:249–259

    Google Scholar 

  • Swearer SE, Caselle JE, Lea DW, Warner RR (1999) Larval retention and recruitment in an island population of a coral-reef fish. Nature 402:799–801

    Article  CAS  Google Scholar 

  • Swearer SE, Shima JS, Hellberg ME, Thorrold SR, Jones GP, Robertson DR, Morgan SG, Selkoe KA, Ruiz GM, Warner RR (2002) Evidence of self-recruitment in demersal marine populations. Bull Mar Sci 70:251–271

    Google Scholar 

  • Swofford DL (1998) PAUP* phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Taylor MS, Hellberg ME (2005) Marine radiations at small geographic scales: speciation in neotropical reef gobies (Elacatinus). Evolution 59:374–385

    Article  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak FFJ, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Article  Google Scholar 

  • Tringali MD, Bert TM, Seyoum S, Bermingham E, Bartolacci D (1999) Molecular phylogenetics and ecological diversification of the transisthmian fish genus Centropomus (Perciformes: Centropomidae). Mol Phylogenet Evol 13:193–207

    Article  PubMed  CAS  Google Scholar 

  • Viñas J, Alvarado Bremer JR, Pla C (2004a) Inter-oceanic genetic differentiation among albacore (Thunnus alalunga) populations. Mar Biol 145:225–232

    Article  CAS  Google Scholar 

  • Viñas J, Alvarado Bremer JR, Pla C (2004b) Phylogeography of the Atlantic bonito (Sarda sarda) in the northern Mediterranean: the combined effects of historical vicariance, population expansion, secondary invasion, and isolation by distance. Mol Phylogenet Evol 33:32–42

    Article  CAS  Google Scholar 

  • Wakeley J (2001) The coalescent in an island model of population subdivision with variation among demes. Theor Popul Biol 59:133–144

    Article  PubMed  CAS  Google Scholar 

  • Wilson DT, McCormick MI (1999) Microstructure of settlement-marks in the otoliths of tropical reef Fishes. Mar Biol 134:29–41

    Article  Google Scholar 

  • Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686–692

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This manuscript was improved by comments from three anonymous reviewers. The authors acknowledge funding and logistic support from The National Geographic Society, The Queensland Government/Smithsonian Institution Collaborative Research Program on Reef Fishes, The Seychelles Fishing Authority, Cocos Keeling and Christmas Island National Parks Department of Environment and Heritage Australia, The Australian Institute of Marine Science, The Lizard Island Research Station and the James Cook University internal funding scheme. Specimens were provided by A. Maypa and A. Alcala (Silliman University Angelo King Centre for Research and Environmental Management, Philippines), M. Meekan (Australian Institute of Marine Sciences), R. Robertson (STRI), J. Ackerman, W. Robbins, M. Srinivasan and G.P. Jones (JCU). This project benefited from discussions with S. Planes, R. Robertson, B. Bowen and G. Russ. The work was carried out under James Cook University Ethics Approval No. A503.

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Klanten, O.S., Choat, J.H. & van Herwerden, L. Extreme genetic diversity and temporal rather than spatial partitioning in a widely distributed coral reef fish. Mar Biol 150, 659–670 (2007). https://doi.org/10.1007/s00227-006-0372-7

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