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, h = 1.0 and nucleotide diversity π = 13.6%). In addition to these unique characteristics, there was no evidence of isolation by distance (r = 0.458, R 2 = 0.210, P = 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, P < 0.05; West Indian–East Indian–Pacific AMOVA Φ st = 0.079, P < 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
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
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
Avise JC (1998) Conservation genetics in the marine realm. J Hered 89:377–382
Barber PH, Palumbi SR, Erdmann MV, Moosa MK (2000) A marine Wallace’s line? Nature 406:692–693
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
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
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
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
Bohonak AJ (2002) IBD (isolation by distance): a program for analyses of isolation by distance. J Hered 93:153–154
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
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
Choat JH, Clements KD (1998) Vertebrate herbivory in marine and terrestrial environments: a nutritional ecology perspective. Annu Rev Ecol Syst 29:375–403
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
Choat JH, Clements KD, Robbins WD (2002) The trophic status of herbivorous fishes on coral reefs. I: dietary analyses. Mar Biol 140:613–623
Choat JH, Robbins WD, Clements KD (2004) The trophic status of herbivorous fishes on coral reefs. Mar Biol 145:445–454
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
Duda TF, Kohn AJ (2005) Species-level phylogeography and evolutionary history of the hyperdiverse marine gastropod genus Conus. Mol Phylogenet Evol 34:257–272
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
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
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
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
Hallam A (1984) Pre-Quaternary sea-level changes. Annu Rev Earth Planet Sci 12:205–243
Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600
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
Helfman GS, Colette BB, Facey DE (1997) The diversity of fishes. Blackwell Science, Massachusetts
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
Huelsenbeck JP, Ronquist F (2001) MR. BAYES: bayesian inference of phylogenetic trees. Bioinformatics 17:754–755
Jones GP, Milicich MJ, Emslie JJ, Lunow C (1999) Self-recruitment in a coral reef fish population. Nature 402:802–804
Kinlan BP, Gaines SD (2003) Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84:2007–2020
Kinlan BP, Gaines SD, Lester SE (2005) Propagule dispersal and the scales of marine community process. Divers Distrib 11:139–148
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
Kuiter RH, Debelius H (2001) Surgeonfishes, rabbitfishes and their relatives. TMC Publishing, Chorleywood
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
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
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
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
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
Li WH (1977) Distribution of nucleotide differences between two randomly chosen cistrons in a finite population. Genetics 85:331–337
McMillan WO, Palumbi SR (1997) Rapid rate of control-region evolution in Pacific Butterflyfishes (Chaetodontidae). J Mol Evol 45:473–484
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
Meyer CP, Geller JB, Paulay G (2005) Fine scale endemism on coral reefs: Archipelagic differentiation in turbinid gastropods. Evolution 59:113–125
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
Munday PL, van Herwerden L, Dudgeon CL (2004) Evidence for sympatric speciation by host shift in the sea. Curr Biol 14:1498–1504
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Nichols RA, Hewitt GM (1994) The genetic consequences of long-distance dispersal during colonization. Heredity 72:312–317
Palumbi SR (1992) Marine speciation on a small planet. Trends Ecol Evol 7:114–118
Palumbi SR (1997) Molecular biogeography of the Pacific. Coral Reefs 16(Suppl.):S47–S52
Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:S146–S158
Palumbi SR (2004) Marine reserves and ocean neighborhoods: the spatial scale of marine populations and their management. Annu Rev Environ Resour 29:31–68
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
Pianka ER (1978) Evolutionary ecology. Harper & Row Publishers, New York
Pickering KT (2000) The Cenozoic world. In: Culver SJ, Rawson PF (eds) Biotic response to global change. Cambridge University Press, Cambridge, pp. 20–34
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
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
Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818
de Queiroz A (2005) The resurrection of oceanic dispersal in historical biogeography. Trends Ecol Evol 20:68–73
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
Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol 20:76–86
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
Robertson DR (1982) Fish feces as fish food on a Pacific coral reef. Mar Ecol Prog Ser 7:253–265
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
Rocha LA, Robertson DR, Roman J, Bowen BW (2005) Ecological speciation in tropical reef fishes. Proc R Soc Lond B 272:573–579
Rogers AR (1995) Genetic evidence for a Pleistocene population explosion. Evolution 49:608–615
Rogers AR, Harpending HC (1992) Population-growth makes waves in the distribution of pairwise genetic-differences. Mol Biol Evol 9:552–569
Sale PF (2002) Coral reef fishes, dynamics and diversity in a complex ecosystem. Academic, San Diego
Sambrook J, Fritsh EF, Maniatis T (1989) Molecular cloning, a laboratory manual. Cold Spring Harbour Laboratory Press, Cold Spring Harbor
Sanderson MJ (1997) A nonparametric approach to estimating divergence times in the absence of rate constancy. Mol Biol Evol 14:1218–1231
Sanderson MJ (2003) r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19:301–302
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
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
Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562
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
Stobutzki IC (1997) Energetic cost of sustained swimming in the late pelagic stages of reef fishes. Mar Ecol Prog Ser 152:249–259
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
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
Swofford DL (1998) PAUP* phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland
Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109
Taylor MS, Hellberg ME (2005) Marine radiations at small geographic scales: speciation in neotropical reef gobies (Elacatinus). Evolution 59:374–385
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
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
Viñas J, Alvarado Bremer JR, Pla C (2004a) Inter-oceanic genetic differentiation among albacore (Thunnus alalunga) populations. Mar Biol 145:225–232
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
Wakeley J (2001) The coalescent in an island model of population subdivision with variation among demes. Theor Popul Biol 59:133–144
Wilson DT, McCormick MI (1999) Microstructure of settlement-marks in the otoliths of tropical reef Fishes. Mar Biol 134:29–41
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
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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DOI: https://doi.org/10.1007/s00227-006-0372-7