Marine Biology

, Volume 156, Issue 4, pp 689–698 | Cite as

Endemism and dispersal: comparative phylogeography of three surgeonfishes across the Hawaiian Archipelago

  • Jeff A. EbleEmail author
  • Robert J. Toonen
  • Brian W. Bowen
Original Paper


To evaluate the hypothesis that a general correlation exists between species range size and dispersal ability, we surveyed mitochondrial cytochrome b sequence variation in three surgeonfish species with vastly different ranges: Ctenochaetus strigosus, Hawaiian endemic, N = 531; Zebrasoma flavescens, North Pacific, N = 560; Acanthurus nigrofuscus, Indo-Pacific, N = 305. Collections were made throughout the 2,500 km expanse of the Hawaiian Archipelago and adjacent Johnston Atoll. Analyses of molecular variance demonstrate that all three species are capable of maintaining population connectivity on a scale of thousands of km (all species global ΦST = NS). However, rank order comparison of pairwise ΦST results and Exact test P-values revealed modest but significantly different patterns of gene flow among the three species surveyed, with the degree of genetic structure increasing as range size decreases (P = 0.001). These results are consistent with mtDNA surveys of four additional Hawaiian reef fauna in which a wide-spread Indo-Pacific species exhibited genetic homogeneity across the archipelago, while three endemics had significant population subdivision over the same range. Taken together, these seven cases invoke the hypothesis that Hawaii’s endemic reef fishes evolved from species with reduced dispersal ability that, after initial colonization, could not maintain contact with parent populations.


Reef Fish Larval Duration Pelagic Larval Duration Hawaiian Archipelago Main Hawaiian Island 



We gratefully acknowledge two anonymous reviewers for helpful comments that much improved the manuscript. In addition, we thank the Papahānaumokuākea Marine National Monument, US Fish and Wildlife Services, and Hawaii Division of Aquatic Resources (DAR) for coordinating research activities and permitting procedures, and the crew of the NOAA Ship Hi’ialakai and B. Walsh, B. Carmen, I. Williams, and S. Cotton of Kona DAR for assistance in the field. This work was funded by a grant to B.W.B. and R. Toonen from the US National Science Foundation (OCE-0454873), by the HIMB-NWHI Coral Reef Research Partnership (NMSP MOA 2005-008/6682) and the National Oceanic and Atmospheric Administration, Center for Sponsored Coastal Ocean Science, under awards #NA05NOS4261157 to the University of Hawaii for the Hawaii Coral Reef Initiative. We thank the staff of the Hawaii Institute of Marine Biology (HIMB) Core Facility for providing sequences. The HIMB core facility is supported by an EPSCoR grant to University of Hawaii (EPS-0554657). J.A.E. was partially funded by the NSF GK-12 Fellowship Program (DGE02-32016). Thanks to T. Daly-Engel, L. Sorenson, L. Basch, A. Alexander, M. Craig, L. Rocha, R. Kosaki, C. Musberger, D. White, C. Meyer, M. Gaither, M. Iacchei, G. Conception, Y. Papastamatiou, M. Crepeau, and Z. Szabo for field collections, laboratory assistance and valuable advice. This is HIMB contribution No. 1333. This study complied with current laws in the United States and were conducted in accordance with the regulations of the University of Hawaii Institutional Animal Care and Use Committee (IACUC).

Supplementary material

227_2008_1119_MOESM1_ESM.doc (288 kb)
Supplementary material 1 (DOC 287 kb)


  1. Allendorf FW, Phelps SR (1981) Use of allelic frequencies to describe population structure. Can J Fish Aquat Sci 38:1507–1514. doi: Google Scholar
  2. Almany GR, Berumen ML, Thorrold SR, Planes S, Jones GP (2007) Local replenishment of coral reef fish populations in a marine reserve. Science 316:742–744. doi: Google Scholar
  3. Bay LK, Crozier RH, Caley MJ (2006) The relationship between population genetic structure and pelagic larval duration in coral reef fishes on the Great Barrier Reef. Mar Biol (Berl) 149:1247–1256. doi: Google Scholar
  4. Bellwood DR, Fisher R (2001) Relative swimming speeds in reef fish larvae. Mar Ecol Prog Ser 211:299–303. doi: Google Scholar
  5. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300Google Scholar
  6. Bird CE, Holland BS, Bowen BW, Toonen RJ (2007) Contrasting phylogeography in three endemic Hawaiian limpets (Cellana spp.) with similar life histories. Mol Ecol 16:3173–3186. doi: PubMedGoogle Scholar
  7. Bohonak AJ (1999) Dispersal, gene flow and population structure. Q Rev Biol 72:21–45. doi: Google Scholar
  8. Bowen BW (1999) Preserving genes, species, or ecosystems? Healing the fractured foundation of conservation policy. Mol Ecol 8:S5–S10. doi: PubMedGoogle Scholar
  9. Bowen BW, Bass AL, Rocha LA, Grant WS, Robertson DR (2001) Phylogeography of the trumpetfishes (Aulostomus): ring species complex on a global scale. Evol Int J Org Evol 55:1029–1039. doi:[1029:POTTAR]2.0.CO;2 Google Scholar
  10. Bowen BW, Bass AL, Muss A, Carlin J, Robertson DR (2006) Phylogeography of two Atlantic squirrelfishes (Family Holocentridae): exploring links between pelagic larval duration and population connectivity. Mar Biol (Berl) 149:899–913. doi: Google Scholar
  11. Bradbury IR, Bentzen P (2007) Non-linear genetic isolation by distance: implications for dispersal estimation in anadromous and marine fish populations. Mar Ecol Prog Ser 340:245–257. doi: Google Scholar
  12. Bradbury IR, Snelgrove PVR (2001) Contrasting larval transport in demersal fish and benthic invertebrates: the roles of behaviour and advective processes in determining spatial pattern. Can J Fish Aquat Sci 58:811–823. doi: Google Scholar
  13. Brown JH, Stevens GC, Kaufman DM (1996) The geographic range: size, shape, boundaries, and internal structure. Annu Rev Ecol Syst 27:597–623. doi: Google Scholar
  14. Clague D (1996) The growth and subsidence of the Hawaiian-emperor volcanic chain. In: Keast A, Miller SE (eds) The origin and evolution of Pacific Island biotas, New Guinea to Eastern Polynesia: patterns and processes. SPB, Amsterdam, pp 35–50Google Scholar
  15. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660. doi: PubMedGoogle Scholar
  16. Cowen RK, Lwiza KMM, Sponaugle S, Paris CB, Olson DB (2000) Connectivity of marine populations: open or closed? Science 287:857–859. doi: Google Scholar
  17. Craig MT, Eble JA, Bowen BW, Robertson DR (2007) High genetic connectivity across the Indian and Pacific Oceans in the reef fish Myripristis berndti (Holocentridae). Mar Ecol Prog Ser 334:245–254. doi: Google Scholar
  18. Crisp DJ (1984) Overview of research on marine invertebrate larvae. In: Costlow JD, Tipper RC (eds) Marine biodeterioration: an interdisciplinary study. Naval Institute Press, Annapolis, pp 103–126Google Scholar
  19. DeMartini EE, Friedlander AM (2004) Spatial patterns of endemism in shallow-water reef fish populations of the Northwestern Hawaiian Islands. Mar Ecol Prog Ser 271:281–296. doi: Google Scholar
  20. Doherty PJ, Planes S, Mather P (1995) Gene flow and larval duration in 7 species of fish from the Great Barrier Reef. Ecology 76:2373–2391. doi: Google Scholar
  21. Domingues VS, Bucciarelli G, Almada VC, Bernardi G (2005) Historical colonization and demography of the Mediterranean damselfish, Chromis chromis. Mol Ecol 14:4051–4063. doi: PubMedGoogle Scholar
  22. Excoffier, Laval LG, Schneider S (2005) Arlequin ver 3.0: An integrated software package for population genetics data analysis. Evol Bio Online 1: 47–50Google Scholar
  23. Fisher R, Leis JM, Clark DL, Wilson SK (2005) Critical swimming speeds of late-stage coral reef fish larvae: variation within species, among species and between locations. Mar Biol (Berl) 147:1201–1212. doi: Google Scholar
  24. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedPubMedCentralGoogle Scholar
  25. Gaston KJ (1994) Rarity. Chapman and Hall, New YorkGoogle Scholar
  26. Gaston KJ (1996) Species-range-size distributions: patterns, mechanisms and implications. Trends Ecol Evol 11:197–201. doi: PubMedGoogle Scholar
  27. Gaylord B, Gaines SD (2000) Temperature or transport? Range limits in marine species mediated solely by flow. Am Nat 155:769–789. doi: PubMedGoogle Scholar
  28. Gerlach G, Atema J, Kingsford MJ, Black KP, Miller-Sims V (2007) Smelling home can prevent dispersal of reef fish larvae. Proc Natl Acad Sci USA 104:858–863. doi: PubMedGoogle Scholar
  29. Grant WS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J Hered 89:415–426. doi: Google Scholar
  30. Halpern BS, Gaines SD, Warner RR (2004) Confounding effects of export of production and the displacement of fishing effort from marine reserves. Ecol Appl 14:1248–1256. doi: Google Scholar
  31. Hart AM, Russ GR (1996) Response of herbivorous fishes to crown-of-thorns starfish Acanthaster planci outbreaks III. Age, growth, mortality and maturity indices of Acanthurus nigrofuscus. Mar Ecol Prog Ser 136:25–35. doi: Google Scholar
  32. Hedgecock D (1986) Is gene flow from pelagic larval dispersal important in the adaptation and evolution of marine-invertebrates. Bull Mar Sci 39:550–564Google Scholar
  33. Hourigan FH, Reese ES (1987) Mid-ocean isolation and the evolution of Hawaiian reef fishes. Trends Ecol Evol 2:187–191. doi: PubMedGoogle Scholar
  34. Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evol Int J Org Evol 53:1898–1914. doi: Google Scholar
  35. Jones GP, Milicich MJ, Emslie MJ, Lunow C (1999) Self-recruitment in a coral reef fish population. Nature 402:802–804. doi: Google Scholar
  36. Jones GP, Planes S, Thorrold SR (2005) Coral reef fish larvae settle close to home. Curr Biol 15:1314–1318. doi: Google Scholar
  37. Kinlan BP, Gaines SD (2003) Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84:2007–2020. doi: Google Scholar
  38. Kruskal WH, Wallis WA (1952) Use of ranks in one-criterion analysis of variance. J Am Stat 47:583–621. doi: Google Scholar
  39. Kunin WE, Gaston KJ (1993) The biology of rarity: patterns, causes and consequences. Trends Ecol Evol 8:298–301. doi: PubMedGoogle Scholar
  40. 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: new insights into their ecology. Academic Press, San Diego, pp 171–199Google Scholar
  41. Lessios HA, Kessing BD, Robertson DR (1998) Massive gene flow across the world’s most potent marine biogeographic barrier. Proc R Soc Lond B Biol Sci 265:583–588. doi: Google Scholar
  42. Lester SE, Ruttenberg BI, Gaines SD, Kinlan BP (2007) The relationship between dispersal ability and geographic range size. Ecol Lett 10:745–758. doi: PubMedGoogle Scholar
  43. Levin LA (2006) Recent progress in understanding larval dispersal: new directions and digressions. Integr Comp Biol 46:282–297. doi: Google Scholar
  44. Lobel PS (2003) Marine life of Johnston Atoll, Central Pacific Ocean. Natural World Press, VidaGoogle Scholar
  45. Meyer CP, Geller JB, Paulay G (2005) Fine scale endemism on coral reefs: archipelagic differentiation in turbinid gastropods. Evol Int J Org Evol 59:113–125Google Scholar
  46. Mora C, Sale PF (2002) Are populations of coral reef fish open or closed? Trends Ecol Evol 17:422–428. doi: Google Scholar
  47. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  48. Palumbi SR (1994) Genetic-divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Evol Syst 25:547–572Google Scholar
  49. Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:S146–S158. doi:[0146:PGDCAT]2.0.CO;2 Google Scholar
  50. Paulay G, Meyer C (2006) Dispersal and divergence across the greatest ocean region: do larvae matter? Integr Comp Biol 46:269–281. doi: PubMedGoogle Scholar
  51. Planes S (2002) Biogeography and larval dispersal inferred from population genetic analysis. In: Sale PF (ed) Coral reef fishes: dynamics and diversity in a complex ecosystem. Academic Press, San Diego, pp 201–220Google Scholar
  52. Planes S, Galzin R, Bonhomme F (1996) A genetic metapopulation model for reef fishes in oceanic islands: the case of the surgeonfish, Acanthurus triostegus. J Evol Biol 9:103–117. doi: Google Scholar
  53. Planes S, Parroni M, Chauvet C (1998) Evidence of limited gene flow in three species of coral reef fishes in the lagoon of New Caledonia. Mar Biol (Berl) 130:361–368. doi: Google Scholar
  54. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818. doi: PubMedPubMedCentralGoogle Scholar
  55. Proebstel DS, Evans RP, Shiozawa DK, Williams RN (1993) Preservation of nonfrozen tissue samples from a salmonine fish Brachymystax lenok (Pallas) for DNA analysis. J Ichthyol 9:9–17Google Scholar
  56. Ramon ML, Nelson PA, DeMartini E, Walsh WJ, Bernardi G (2008) Phylogeography, historical demography, and the role of post-settlement ecology in two Hawaiian damselfish species. Mar Biol (Berl) 153:1207–1217. doi: Google Scholar
  57. Randall JE (1998) Zoogeography of shore fishes of the Indo-Pacific region. Zool Stud 37:227–268Google Scholar
  58. Randall JE (2007) Reef and shore fishes of the Hawaiian Islands. University of Hawaii Press, HonoluluGoogle Scholar
  59. Randall JE, Clements KD (2001) Second revision of the surgeonfish genus Ctenochaetus (Perciformes: Acanthuridae), with descriptions of two new species. Indo-Pac Fish 32:1–33Google Scholar
  60. Raymond M, Rousset F (1995) An exact test for population differentiation. Evol Int J Org Evol 49:1280–1283. doi: Google Scholar
  61. Riginos C, Victor BC (2001) Larval spatial distributions and other early life-history characteristics predict genetic differentiation in eastern Pacific blennioid fishes. Proc R Soc Lond B Biol Sci 268:1931–1936. doi: Google Scholar
  62. Rivera MAJ, Kelley CD, Roderick GK (2004) Subtle population genetic structure in the Hawaiian grouper, Epinephelus quernus (Serranidae) as revealed by mitochondrial DNA analyses. Biol J Linn Soc Lond 81:449–468. doi: Google Scholar
  63. Robertson DR, Grove JS, McCosker JE (2004) Tropical transpacific shore fishes. Pac Sci 58:507–565. doi: Google Scholar
  64. 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. doi: Google Scholar
  65. Rocha LA, Robertson DR, Roman J, Bowen BW (2005) Ecological speciation in tropical reef fishes. Proc R Soc B 272:573–579PubMedGoogle Scholar
  66. Roughgarden J, Iwasa Y, Baxter C (1985) Demographic theory for an open marine population with space-limited recruitment. Ecology 66:54–67. doi: Google Scholar
  67. Ryman N, Palm S, Andre C, Carvalho GR, Dahlgren TH, Jorde PE, Laikre L, Larson LC, Palme A, Ruzzante DE (2006) Power for detecting genetic divergence: differences between statistical methods and marker loci. Mol Ecol 15:2031–2045. doi: PubMedGoogle Scholar
  68. Sale PF, Kritzer JP (2003) Determining the extent and spatial scale of population connectivity: decapods and coral reef fishes compared. Fish Res 65:153–172. doi: Google Scholar
  69. Scheltema RS (1971) Larval dispersal as a means of genetic exchange between geographically separated population of shallow-water benthic marine gastropods. Bull Mar Sci 140:284–322Google Scholar
  70. Scheltema RS (1986) On dispersal and planktonic larvae of benthic invertebrates—an eclectic overview and summary of problems. Bull Mar Sci 39:290–322Google Scholar
  71. Shanks AL, Grantham BA, Carr MH (2003) Propagule dispersal distance and the size and spacing of marine reserves. Ecol Appl 13:S159–S169. doi:[0159:PDDATS]2.0.CO;2 Google Scholar
  72. Shields GF, Gust JR (1995) Lack of geographic structure in mitochondrial DNA sequences of Bering Sea walley pollock, Theragra chalcogramma. Mol Mar Biol Biotechnol 4:69–82PubMedGoogle Scholar
  73. Shuto T (1974) Larval ecology of prosobranch gastropods and its bearing on biogeography and paleontology. Lethaia 7:239–256. doi: Google Scholar
  74. Siegel DA, Kinlan BP, Gaylord B, Gaines SD (2003) Lagrangian descriptions of marine larval dispersion. Mar Ecol Prog Ser 260:83–96. doi: Google Scholar
  75. Song CB, Near TJ, Page JM (1998) Phylogenetic relations among Percid fishes as inferred from mitochondrial cytochrome b DNA sequence data. Mol Phylogenet Evol 10:343–353. doi: PubMedGoogle Scholar
  76. Strathmann RR (1993) Hypotheses on the origins of marine larvae. Annu Rev Ecol Syst 24:89–117. doi: Google Scholar
  77. Sunnucks P, Hales DF (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I–II in aphids of the genus Sitobion (Hemiptera: Aphididae). Mol Biol Evol 13:510–524PubMedGoogle Scholar
  78. Swearer SE, Caselle JE, Lea DW, Warner RR (1999) Larval retention and recruitment in an island population of a coral-reef fish. Nature 402:799–802. doi: Google Scholar
  79. Swearer SE, Shima JS, Hellberg ME et al (2002) Evidence of self-recruitment in demersal marine populations. Bull Mar Sci 70:251–271Google Scholar
  80. Taberlet P, Meyer A, Bouvert J (1992) Unusually large mitochondrial variation in populations of the blue tit, Parus caeruleus. Mol Ecol 1:27–36. doi: PubMedGoogle Scholar
  81. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526PubMedGoogle Scholar
  82. Thorson G (1950) Reproductive and larval ecology of marine bottom invertebrates. Biol Rev Camb Philos Soc 25:1–45. doi: PubMedGoogle Scholar
  83. Thresher RE (1984) Reproduction in reef fishes. TFH, Neptune CityGoogle Scholar
  84. Victor BC, Wellington GM (2000) Endemism and pelagic larval duration of reef fishes in the eastern Pacific Ocean. Mar Ecol Prog Ser 205:241–248. doi: Google Scholar
  85. Walsh WJ (1987) Patterns of recruitment and spawning in Hawaiian reef fishes. Environ Biol Fish 18:257–276. doi: Google Scholar
  86. Waples RS, Rosenblatt RH (1987) Patterns of larval drift in southern California marine shore fishes inferred from allozyme data. Fish B-NOAA 85:1–11Google Scholar
  87. Warner RR, Hughes TP (1988) The population dynamics of reef fishes. In: proceedings of the 6th International Coral Reef Symposium. Townsville, pp 149–155Google Scholar
  88. Zar JH (1999) Biostatistical analysis. Prentice-Hall, New JerseyGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Jeff A. Eble
    • 1
    Email author
  • Robert J. Toonen
    • 1
  • Brian W. Bowen
    • 1
  1. 1.Hawaii Institute of Marine BiologyKaneoheUSA

Personalised recommendations