Oceanic dispersal in a sedentary reef shark (Triaenodon obesus): Genetic evidence for extensive connectivity without a pelagic larval stage

Journal of Biogeography

Volumn 39, Issue 6, 2012, Pages 1144-1156

  Whitney, Nicholas M ^a   Robbins, William D ^b,c   Schultz, Jennifer K ^a,d   Bowen, Brian W ^a   Holland, Kim N ^a  

^a UNIVERSITY OF HAWAII   (United States)

^b JAMES COOK UNIVERSITY   (Australia)

^c Wildlife Marine   (Australia)

^d NATIONAL MARINE FISHERIES SERVICE   (United States)

Author keywords

Control region; Dispersal; East Pacific Barrier; Elasmobranch; Indo Pacific Barrier; Marine biogeography; Marine fish; MtDNA; Phylogeography

Indexed keywords

ARCHIPELAGO; COLONIZATION; COMMON ANCESTRY; CONNECTIVITY; DISPERSAL; EVOLUTIONARY BIOLOGY; GENETIC ANALYSIS; GENETIC VARIATION; HABITAT TYPE; ISOLATED POPULATION; LARVA; MITOCHONDRIAL DNA; PHYLOGENY; PHYLOGEOGRAPHY; POPULATION DISTRIBUTION; POPULATION GENETICS; REEF; SHARK; SPATIAL ANALYSIS; ZOOGEOGRAPHY;

AUSTRALIA; CORAL SEA; GREAT BARRIER REEF; HAWAIIAN ISLANDS; INDIAN OCEAN; PACIFIC OCEAN; PACIFIC OCEAN (CENTRAL); PACIFIC OCEAN (EAST); PACIFIC OCEAN (TROPICAL); QUEENSLAND;

CARCHARHINUS SPRINGERI; CHONDRICHTHYES; OSTEICHTHYES; PISCES; TELEOSTEI; TRIAENODON OBESUS;

EID: 84861183968     PISSN: 03050270     EISSN: 13652699     Source Type: Journal    
DOI: 10.1111/j.1365-2699.2011.02660.x     Document Type: Article

References (83)

1. 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.
2. Bellwood, D.R. & Wainwright, P.C. (2002) The history and biogeography of fishes on coral reefs. Coral reef fishes: dynamics and diversity in a complex ecosystem (ed. by P.F. Sale ), pp. 5-32. Academic Press, San Diego, CA.
3. Bohonak, A.J. (1999) Dispersal, gene flow, and population structure. Quarterly Review of Biology, 74, 21-45.
4. Bonfil, R., Meyer, M., Scholl, M.C., Johnson, R., O'Brien, S., Oosthuizen, S., Swanson, S., Kotze, D. & Paterson, M. (2005) Transoceanic migration, spatial dynamics, and population linkages of white sharks. Science, 310, 100-103.
5. Bowen, B.W. & Karl, S.A. (2007) Population genetics and phylogeography of sea turtles. Molecular Ecology, 16, 4886-4907.
6. Bowen, B.W., Clark, A.M., Abreu-Grobois, F.A., Chaves, A., Reichart, H. & Ferl, R.J. (1998) Global phylogeography of the ridley sea turtles (Lepidochelys spp.) inferred from mitochondrial DNA sequences. Genetica, 101, 179-189.
7. Bradshaw, C.J.A., Hindell, M.A., Sumner, M.D. & Michael, K.J. (2004) Loyalty pays: potential life history consequences of fidelity to marine foraging regions by southern elephant seals. Animal Behaviour, 68, 1349-1360.
8. Briggs, J.C. (1966) Zoogeography and evolution. Evolution, 20, 282-289.
9. Briggs, J.C. (1974) Marine zoogeography. McGraw-Hill, New York.
10. Briggs, J.C. (1999) Coincident biogeographic patterns: Indo-West Pacific Ocean. Evolution, 53, 326-335.
11. Briggs, J.C. (2005) The marine East Indies: diversity and speciation. Journal of Biogeography, 32, 1517-1522.
12. Cappetta, H. (1987) Chondrichthyes II: Mesozoic and Cenozoic Elasmobranchii. Handbook of Paleoichthyology, Vol. 3B (ed. by H.P. Schultze ). Verlag, Munich.
13. Carson, H.L. & Clague, D.A. (1995) Geology and biogeography of the Hawaiian Islands. Hawaiian biogeography: evolution in a hotspot archipelago (ed. by W. Wagner and V. Funk ), pp. 14-29. Smithsonian Institution Press, Washington, DC.
14. Castro, A.L.F., Stewart, B.S., Wilson, S.G., Hueter, R.E., Meekan, M.G., Motta, P.J., Bowen, B.W. & Karl, S.A. (2007) Population genetic structure of Earth's largest fish, the whale shark (Rhincodon typus). Molecular Ecology, 16, 5183-5192.
15. Chabot, C.L. & Allen, L.G. (2009) Global population structure of the tope (Galeorhinus galeus) inferred by mitochondrial control region sequence data. Molecular Ecology, 18, 545-552.
16. Clague, D.A. & Dalrymple, G.B. (1987) Tectonics, geochronology and origin of the Hawaiian-Emperor volcanic chain. Volcanism in Hawaii (ed. by R.W. Decker, T.L. Wright and P.H. Stauffer ), pp. 1-54. US Government Printing Office, Washington, DC.
17. Clement, M., Posada, D. & Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657-1659.
18. Compagno, L.J.V. (1984) FAO species catalogue, Vol. 4. Sharks of the world: an annotated and illustrated catalogue of shark species known to date. FAO Fisheries Synopsis No. 125. United Nations Development Programme/Food and Agriculture Organization of the United Nations, Rome.
19. Cowen, R., Paris, C. & Srinivasan, A. (2006) Scaling of connectivity in marine populations. Science, 311, 522-527.
20. Craig, M.T., Eble, J.A., Bowen, B.W. & Robertson, D.R. (2007) High genetic connectivity across the Indian and Pacific Oceans in the reef fish Myripristis berndti (Holocentridae). Marine Ecology Progress Series, 334, 245-254.
21. Craig, M.T., Eble, J.A. & Bowen, B.W. (2010) Origins, ages, and populations histories: comparative phylogeography of endemic Hawaiian butterflyfishes (genus Chaetodon). Journal of Biogeography, 37, 2125-2136.
22. Dethmers, K.E.M., Broderick, D., Moritz, C., FitzSimmons, N.N., Limpus, C.J., Lavery, S., Whiting, S., Guinea, M., Prince, R.I.T. & Kennett, R. (2006) The genetic structure of Australasian green turtles (Chelonia mydas): exploring the geographical scale of genetic exchange. Molecular Ecology, 15, 3931-3946.
23. Dudgeon, C.L., Broderick, D. & Ovenden, J.R. (2009) IUCN classification zones concord with, but underestimate, the population genetic structure of the zebra shark Stegostoma fasciatum in the Indo-West Pacific. Molecular Ecology, 18, 248-261.
24. Duncan, K.M., Martin, A.P., Bowen, B.W. & de Couet, H.G. (2006) Global phylogeography of the scalloped hammerhead shark (Sphyrna lewini). Molecular Ecology, 15, 2239-2251.
25. Dupanloup, I., Schneider, S. & Excoffier, L. (2002) A simulated annealing approach to define the genetic structure of populations. Molecular Ecology, 11, 2571-2581.
26. Eble, J.A., Toonen, R.J. & Bowen, B.W. (2009) Endemism and dispersal: comparative phylogeography of three surgeonfishes across the Hawaiian Archipelago. Marine Biology, 156, 689-698.
27. Eckert, S.A. & Stewart, B.S. (2001) Telemetry and satellite tracking of whale sharks, Rhincodon typus, in the Sea of Cortez, Mexico, and the north Pacific Ocean. Environmental Biology of Fishes, 60, 299-308.
28. Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequin (version 3.1): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47-50.
29. Fleminger, A. (1986) The Pleistocene equatorial barrier between the Indian and Pacific Oceans and a likely cause for Wallace's line. UNESCO Technical Papers in Marine Science, 49, 84-97.
30. Friedlander, A.M. & Demartini, E.E. (2002) Contrasts in density, size, and biomass of reef fishes between the northwestern and the main Hawaiian Islands: the effects of fishing down apex predators. Marine Ecology Progress Series, 230, 253-265.
31. Gaida, I.H. (1997) Population structure of the Pacific angel shark, Squatina californica (Squatiniformes: Squatinidae), around the California Channel Islands. Copeia, 1997, 738-744.
32. Gaither, M.R., Toonen, R.J., Robertson, D.R., Planes, S. & Bowen, B.W. (2010) Genetic evaluation of marine biogeographical barriers: perspectives from two widespread Indo-Pacific snappers (Lutjanus kasmira and Lutjanus fulvus). Journal of Biogeography, 37, 133-147.
33. 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. BMC Evolutionary Biology, 11, 189, doi:
34. Heist, E.J. (1999) A review of population genetics in sharks. American Fisheries Society Symposium, 23, 139-146.
35. Heist, E.J. (2005) Genetics: stock identification. Management techniques for elasmobranch fisheries (ed. by J.A. Musick and R. Bonfil ), pp. 62-75. FAO, Fishery Industries Division, Rome.
36. Heupel, M.R., Simpfendorfer, C.A. & Hueter, R.E. (2003) Running before the storm: blacktip sharks respond to falling barometric pressure associated with Tropical Storm Gabrielle. Journal of Fish Biology, 63, 1357-1363.
37. Heupel, M.R., Williams, A.J., Welch, D.J., Ballagh, A., Mapstone, B.D., Carlos, G., Davies, C. & Simpfendorfer, C.A. (2009) Effects of fishing on tropical reef associated shark populations on the Great Barrier Reef. Fisheries Research, 95, 350-361.
38. Heupel, M.R., Simpfendorfer, C.A. & Fitzpatrick, R. (2010) Large-scale movement and reef fidelity of grey reef sharks. PLoS ONE, 5, 1-5.
39. Hoelzel, A.R., Shivji, M.S., Magnussen, J. & Francis, M.P. (2006) Low worldwide genetic diversity in the basking shark (Cetorhinus maximus). Biology Letters, 2, 639-642.
40. Horne, J.B., van Herwerden, L., Choat, J.H. & Robertson, D.R. (2008) High population connectivity across the Indo-Pacific: congruent lack of phylogeographic structure in three reef fish congeners. Molecular Phylogenetics and Evolution, 49, 629-638.
41. 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.
42. Jokiel, P. & Martinelli, F.J. (1992) The vortex model of coral reef biogeography. Journal of Biogeography, 19, 449-458.
43. Jorgensen, S.J., Reeb, C.A., Chapple, T.K., Anderson, S., Perle, C., Van Sommeran, S.R., Fritz-Cope, C., Brown, A.C., Klimley, A.P. & Block, B.A. (2010) Philopatry and migration of Pacific white sharks. Proceedings of the Royal Society B: Biological Sciences, 277, 679-688.
44. Keeney, D.B. & Heist, E.J. (2006) Worldwide phylogeography of the blacktip shark (Carcharhinus limbatus) inferred from mitochondrial DNA reveals isolation of Western Atlantic populations coupled with recent Pacific dispersal. Molecular Ecology, 15, 3669-3679.
45. Keeney, D.B., Heupel, M.R., Heuter, R.E. & Heist, E.J. (2003) Genetic heterogeneity among blacktip shark, Carcharhinus limbatus, continental nurseries along the U.S. Atlantic and Gulf of Mexico. Marine Biology, 143, 1039-1046.
46. Kohler, N.E., Casey, J.G. & Turner, P.A. (1998) NMFS cooperative shark tagging program, 1962-93: an atlas of shark tag and recapture data. Marine Fisheries Review, 60, 1-87.
47. Kohler, N.E., Natanson, L.J., Pratt, H.L.J., Turner, P.A. & Briggs, R. (1999) The shark tagger - 1998 annual summary. National Marine Fisheries Service, Narragansett, RI.
48. Leriche, M. (1910) Les poissons tertiaires de la belgique. III. Le poissons oligocènes. Mémoires du Musée Royal d'Histoire Naturelle de Belgique, 3, 49-228.
49. Lester, S.E., Ruttenberg, B.I., Gaines, S.D. & Kinland, B.P. (2007) The relationship between dispersal ability and geographic range size. Ecological Letters, 10, 745-758.
50. Lewallen, E.A., Anderson, T.W. & Bohonak, A.J. (2007) Genetic structure of leopard shark (Triakis semifasciata) populations in California waters. Marine Biology, 152, 599-609.
51. Lourie, S.A. & Vincent, A.C.J. (2004) A marine fish follows Wallace's Line: the phylogeography of the three-spot seahorse (Hippocampus trimaculatus, Syngnathidae, Teleostei) in Southeast Asia. Journal of Biogeography, 31, 1975-1985.
52. Manni, F., Guerard, E. & Heyer, E. (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by Monmonier's algorithm. Human Biology, 76, 173-190.
53. Mora, C., Chittaro, P.M., Sale, P.F., Kritzer, J.P. & Ludsin, S.A. (2003) Patterns and processes in reef fish diversity. Nature, 421, 933-936.
54. Musick, J.A., Harbin, M.M. & Compagno, L.J.V. (2004) Historical zoogeography of the Selachii. Biology of sharks and their relatives (ed. by J.C. Carrier, J.A. Musick and M.R. Heithaus ), pp. 42-105. CRC Press, Boca Raton, FL.
55. Nelson, D.R. & Johnson, R.H. (1980) Behaviour of the reef sharks of Rangiroa, French Polynesia. National Geographic Society Research Report, 12, 479-499.
56. Nelson, J.S., Hoddell, R.J., Chou, L.M., Chan, W.K. & Phang, V.P.E. (2000) Phylogeographic structure of false clownfish, Amphiprion ocellaris, explained by sea level changes on the Sunda shelf. Marine Biology, 137, 727-736.
57. Ochoa-Lopez, E., Villavicencio-Garayzar, C.J. & Ruiz-Gaytan, A. (1997) First record of whitetip reef shark, Triaenodon obesus in the west coast of México (Revillagigedo Archipelago). Revista de Biologia Tropical, 44/45, 687-688.
58. Ovenden, J.R., Kashiwagi, T., Broderick, D., Giles, J. & Salini, J. (2009) The extent of population genetic subdivision differs among four co-distributed shark species in the Indo-Australian archipelago. BMC Evolutionary Biology, 9, 40.
59. Portnoy, D.S., McDowell, J., Heist, E.J., Musick, J.A. & Graves, J.E. (2010) World phylogeography and male-mediated gene flow in the sandbar shark, Carcharhinus plumbeus. Molecular Ecology, 19, 1994-2010.
60. Purdy, R.W., Schneider, V.P., Applegate, S.P., Mclellan, J.H., Meyer, R.L. & Slaughter, B.H. (2001) The neogene sharks, rays, and bony fishes from Lee Creek mine, Aurora, North Carolina. Smithsonian Contributions to Paleobiology, 90, 71-202.
61. Ramon, M.L., Nelson, P.A., Demartini, E.E., Walsh, W.J. & Bernardi, G. (2008) Phylogeography, historical demography, and the role of post-settlement ecology in two Hawaiian damselfish species. Marine Biology, 153, 1207-1217.
62. Randall, J.E. (1977) Contribution to the biology of the whitetip reef shark (Triaenodon obesus). Pacific Science, 31, 143-164.
63. Reece, J.S., Bowen, B.W., Joshi, K., Goz, V. & Larson, A. (2010) Phylogeography of two moray eels indicates high dispersal throughout the Indo-Pacific. Journal of Heredity, 101, 391-402.
64. Reinecke, T., Moths, H., Grant, A. & Breikreutz, H. (2005) Die Elasmobranchier des norddeutschen Chattiums, insbesondere des Sternberger Gesteins (Eochattium, Oberes Oligozän). Palaeontos, 8, 1-135.
65. Robbins, W.D. (2006a) Abundance, demography, and population structure of the grey reef shark (Carcharhinus amblyrhynchos) and the whitetip reef sharks (Triaenodon obesus) (fam. Carcharhinidae). PhD Thesis, James Cook University, Townsville, Qld.
66. Robbins, W.D. (2006b) Evaluation of two underwater biopsy probes for in situ collection of shark tissue samples. Marine Ecology Progress Series, 310, 213-217.
67. Robbins, W.D., Hisano, M., Connolly, S.R. & Choat, J.H. (2006) Ongoing collapse of coral-reef shark populations. Current Biology, 16, 2314-2319.
68. Rocha, L.A., Craig, M.T. & Bowen, B.W. (2007) Phylogeography and the conservation of coral reef fishes. Coral Reefs, 26, 501-512.
69. Rogers, A.R. & Harpending, H. (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution, 9, 552-569.
70. Schneider, S. & Excoffier, L. (1999) Estimation of demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics, 152, 1079-1089.
71. Schrey, A.W. & Heist, E.J. (2003) Microsatellite analysis of population structure in the shortfin mako (Isurus oxyrinchus). Canadian Journal of Fisheries and Aquatic Sciences, 60, 670-675.
72. Schultz, J.K., Feldheim, K.A., Gruber, S.H., Ashley, M.V., Mcgovern, T.M. & Bowen, B.W. (2008) Global phylogeography and seascape genetics of the lemon sharks (genus Negaprion). Molecular Ecology, 17, 5336-5348.
73. Seutin, G., White, B.N. & Boag, P.T. (1991) Preservation of avian and blood tissue samples for DNA analyses. Canadian Journal of Zoology, 69, 82-92.
74. Taylor, L.C. (1993) Sharks of Hawaii: their biology and cultural significance. University of Hawaii Press, Honolulu, HI.
75. Theisen, T.C., Bowen, B.W., Lanier, W. & Baldwin, J.D. (2008) High connectivity on a global scale in the pelagic wahoo, Acanthocybium solandri (tuna family Scombridae). Molecular Ecology, 17, 4233-4247.
76. Thiel, M. & Gutow, M. (2005) The ecology of rafting in the marine environment. II. The rafting organisms and community. Oceanography and Marine Biology: An Annual Review, 43, 279-418.
77. Toonen, R.J., Andrews, K.R., Baums, I.B., Bird, C.E., Concepcion, C.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. & Bowen, B.W. (2011) Defining boundaries for applying ecosystem-based management: a multispecies case study of marine connectivity across the Hawaiian Archipelago. Journal of Marine Biology. Article ID 460173.
78. Voris, H.K. (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. Journal of Biogeography, 27, 1153-1167.
79. Ward, D.J. & Bonavia, C.G. (2001) Additions to, and a review of, the Miocene shark and ray fauna of Malta. Central Mediterranean Naturalist, 3, 131-146.
80. Weir, B.S. & Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358-1370.
81. Whitney, N.M. (2009) Movements, reproductive behaviour, and phylogeography of the whitetip reef shark, Triaenodon obesus. PhD Thesis, University of Hawaii at Manoa, Honolulu, HI.
82. Whitney, N.M., Papastamatiou, Y.P., Holland, K.N. & Lowe, C.G. (2007) Use of an acceleration data logger to measure diel activity patterns in captive whitetip reef sharks, Triaenodon obesus. Aquatic Living Resources, 20, 299-305.
83. Whitney, N.M., Pyle, R.L., Holland, K.N. & Barcz, J.T. (2012) Movements, philopatry, and reproductive seasonality in the whitetip reef shark (Triaenodon obesus) from community-based photo-identification. Environmental Biology of Fishes, 93, 121-136.