A bridge too far: dispersal barriers and cryptic speciation in an Arabian Peninsula grouper (Cephalopholis hemistiktos)
Corresponding Author
Mark A. Priest
Marine Spatial Ecology Lab, School of Biological Sciences, University of Queensland, St Lucia, QLD, 4072 Australia
Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal, 23955-6900 Saudi Arabia
Correspondence: Mark A. Priest, Marine Spatial Ecology Lab, University of Queensland, St. Lucia, QLD 4072, Australia.
E-mail: [email protected]
Search for more papers by this authorJoseph D. DiBattista
Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal, 23955-6900 Saudi Arabia
Department of Environment and Agriculture, Curtin University, Perth, WA 6845, Australia
Search for more papers by this authorJennifer L. McIlwain
Department of Environment and Agriculture, Curtin University, Perth, WA 6845, Australia
Search for more papers by this authorBrett M. Taylor
College of Marine and Environmental Science, James Cook University, Townsville, QLD, 4811 Australia
Search for more papers by this authorNigel E. Hussey
Great Lakes Institute for Environmental Research, University of Windsor, Windsor, ON, N9B 3P4 Canada
Search for more papers by this authorMichael L. Berumen
Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal, 23955-6900 Saudi Arabia
Search for more papers by this authorCorresponding Author
Mark A. Priest
Marine Spatial Ecology Lab, School of Biological Sciences, University of Queensland, St Lucia, QLD, 4072 Australia
Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal, 23955-6900 Saudi Arabia
Correspondence: Mark A. Priest, Marine Spatial Ecology Lab, University of Queensland, St. Lucia, QLD 4072, Australia.
E-mail: [email protected]
Search for more papers by this authorJoseph D. DiBattista
Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal, 23955-6900 Saudi Arabia
Department of Environment and Agriculture, Curtin University, Perth, WA 6845, Australia
Search for more papers by this authorJennifer L. McIlwain
Department of Environment and Agriculture, Curtin University, Perth, WA 6845, Australia
Search for more papers by this authorBrett M. Taylor
College of Marine and Environmental Science, James Cook University, Townsville, QLD, 4811 Australia
Search for more papers by this authorNigel E. Hussey
Great Lakes Institute for Environmental Research, University of Windsor, Windsor, ON, N9B 3P4 Canada
Search for more papers by this authorMichael L. Berumen
Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal, 23955-6900 Saudi Arabia
Search for more papers by this authorAbstract
Aim
We use genetic and age-based analyses to assess the evidence for a biogeographical barrier to larval dispersal in the yellowfin hind, Cephalopholis hemistiktos, a commercially important species found across the Arabian Peninsula.
Location
Red Sea, Gulf of Aden, Gulf of Oman and Arabian Gulf.
Methods
Mitochondrial DNA cytochrome-c oxidase subunit-I and nuclear DNA (S7) sequences were obtained for C. hemistiktos sampled throughout its distributional range. Phylogeographical and population-level analyses were used to assess patterns of genetic structure and to identify barriers to dispersal. Concurrently, age-based demographic analyses using otoliths determined differences in growth and longevity between regions.
Results
Our analyses revealed significant genetic structure congruent with growth parameter differences observed across sampling sites, suggesting cryptic speciation between populations in the Red Sea and Gulf of Aden versus the Gulf of Oman and Arabian Gulf. Coalescence analyses indicated these two regions have been isolated for > 800,000 years.
Main conclusions
Our results indicate historical disruption to gene flow and a contemporary dispersal barrier in the Arabian Sea, which C. hemistiktos larvae are unable to effectively traverse. This provides yet another example of a (cryptic) species with high dispersive potential whose range is delimited by a lack of suitable habitat between locations or an inability to successfully recruit at the range edge.
Supporting Information
Filename | Description |
---|---|
jbi12681-sup-0001-AppendixS1-S3.docxWord document, 410.4 KB | Appendix S1 Summary of morphometric differences between two populations of C. hemistiktos from Randall & Ben-Tuvia (1983). Appendix S2 Phylogenetic relationship among mtDNA COI haplotypes for Cephalopholis hemistiktos and 11 other Cephalopholis species. Appendix S3 Reproductive timing of C. hemistiktos sampled from the coast of northern Oman. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Almany, G.R., Berumen, M.L., Thorrold, S.R., Planes, S. & Jones, G.P. (2007) Local replenishment of coral reef fish populations in a marine reserve. Science, 316, 742–744.
- Almany, G.R., Hamilton, R.J., Bode, M., Matawai, M., Potuku, T., Saenz-Agudelo, P., Planes, S., Berumen, M.L., Rhodes, K.L., Thorrold, S.R., Russ, G.R. & Jones, G.P. (2013) Dispersal of grouper larvae drives local resource sharing in a coral reef fishery. Current Biology, 23, 626–630.
- Asgharian, H., Sahafi, H.H., Ardalan, A.A., Shekarriz, S. & Elahi, E. (2011) Cytochrome c oxidase subunit 1 barcode data of fish of the Nayband National Park in the Persian Gulf and analysis using meta-data flag several cryptic species. Molecular Ecology Resources, 11, 461–472.
- Bandelt, H.J., Forster, P. & Röhl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48.
- Benjamini, Y., Krieger, A.M. & Yekutieli, D. (2006) Adaptive linear step-up procedures that control the false discovery rate. Biometrika, 93, 491–507.
- Berumen, M.L. (2005) The importance of juveniles in modelling growth: butterflyfish at Lizard Island. Environmental Biology of Fishes, 72, 409–413.
- Berumen, M.L., Hoey, A.S., Bass, W.H., Bouwmeester, J., Catania, D., Cochran, J.E.M., Khahil, M.T., Miyake, S., Mughal, M.R., Spaet, J.L.Y. & Saenz-Agudelo, P. (2013) The status of coral reef ecology research in the Red Sea. Coral Reefs, 32, 737–748.
- Botsford, L.W., Micheli, F. & Hastings, A. (2003) Principles for the design of marine reserves. Ecological Applications, 13, 25–31.
- Bowen, B.W., Rocha, L.A., Toonen, R.J., Karl, S.A., Craig, M.T., DiBattista, J.D., Eble, J.A., Gaither, M.R., Skillings, D. & Bird, C.E. (2013) The origins of tropical marine biodiversity. Trends in Ecology and Evolution, 28, 359–366.
- Briggs, J.C. & Bowen, B.W. (2012) A realignment of marine biogeographic provinces with particular reference to fish distributions. Journal of Biogeography, 39, 12–30.
- Burgess, S.C., Nikols, K.J., Gresemer, C.D., Barnett, L.A.K., Derick, A.G., Satterthwaite, E.V., Yamane, L., Morgan, S.G., White, J.W. & Botsford, L.W. (2014) Beyond connectivity: how empirical methods can quantify population persistence to improve marine protected-area design. Ecological Applications, 24, 257–270.
- Chow, S. & Hazama, K. (1998) Universal PCR primers for S7 ribosomal protein gene introns in fish. Molecular Ecology, 7, 1255–1256.
- Clark, P.U., Archer, D., Pollard, D., Blum, J.D., Rial, J.A., Brovkin, V., Mix, A.C., Pisias, N.G. & Roy, M. (2006) The middle Pleistocene transition: characteristics, mechanisms, and implications for long-term changes in atmospheric pCO2. Quaternary Science Reviews, 25, 3150–3184.
- Coles, S.L. (2003) Coral species diversity and environmental factors in the Arabian Gulf and the Gulf of Oman: a comparison to the Indo-Pacific region. Atoll Research Bulletin, 507, 1–19.
10.5479/si.00775630.507.1 Google Scholar
- Coles, S.L. & Wilson, S.C. (2001) Environmental factors affecting reef corals in Oman: a comparison to the Indo-Pacific region. Proceedings of the 1st International Conference on fisheries, aquaculture and environment in the Northwest Indian Ocean (ed. by S. Goddard, H. Al-Oufi, J.L. McIlwain and M.C. Claereboudt), Vol. 2, pp. 133–145. Sultan Qaboos University, Muscat, Oman.
- Craig, M.T., Sadovy de Mitcheson, Y.J. & Heemstra, P.C. (2011) Groupers of the world: a field and market guide. NISC (Pty) Ltd, Grahamstown, South Africa.
- Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772.
- DiBattista, J.D., Wilcox, C., Craig, M.T., Rocha, L.A. & Bowen, B.W. (2011) Phylogeography of the pacific blueline surgeonfish, Acanthurus nigroris, reveals high genetic connectivity and a cryptic endemic species in the Hawaiian archipelago. Journal of Marine Biology, 2011, 1–17.
10.1155/2011/839134 Google Scholar
- DiBattista, J.D., Waldrop, E., Bowen, B.W., Schultz, J.K., Gaither, M.R., Pyle, R.L. & Rocha, L.A. (2012) Twisted sister species of pygmy angelfishes: discordance between taxonomy, coloration, and phylogenetics. Coral Reefs, 31, 839–851.
- DiBattista, J.D., Berumen, M.L., Gaither, M.R., Rocha, L.A., Eble, J.A., Choat, J.H., Craig, M.T., Skillings, D.J. & Bowen, B.W. (2013) After continents divide: comparative phylogeography of reef fishes from the Red Sea and Indian Ocean. Journal of Biogeography, 40, 1170–1181.
- DiBattista, J.D., Rocha, L.A., Hobbs, J.-P.A., He, S., Priest, M.A., Sinclair-Taylor, T.H., Bowen, B.W. & Berumen, M.L. (2015a) When biogeographical provinces collide: hybridization of reef fishes at the crossroads of marine biogeographical provinces in the Arabian Sea. Journal of Biogeography, doi:10.1111/jbi.12526.
- DiBattista, J.D., Waldrop, E., Rocha, L.A., Craig, M.T., Berumen, M.L. & Bowen, B.W. (2015b) Blinded by the bright: a lack of congruence between colour morph and phylogeography for a cosmopolitan Indo-Pacific butterflyfish, Chaetodon auriga. Journal of Biogeography, 42, 1919–1929.
- DiBattista, J.D., Choat, J.H., Gaither, M.R., Hobbs, J.P., Lozano-Cortés, D.F., Myers, R., Paulay, G., Rocha, L.A., Toonen, R.J., Westneat, M. & Berumen, M.L. (in press-a) On the origin of endemic species in the Red Sea. Journal of Biogeography. doi: 10.1111/jbi.12631.
10.1111/jbi.12631 Google Scholar
- DiBattista, J.D., Roberts, M., Bouwmeester, J. et al. (in press-b) A review of contemporary patterns of endemism for shallow water reef fauna in the Red Sea. Journal of Biogeography. doi: 10.1111/jbi.12649.
10.1111/jbi.12649 Google Scholar
- Drew, J., Allen, G.R., Kaufman, L. & Barber, P.H. (2008) Endemism and regional color and genetic differences in five putatively cosmopolitan reef fishes. Conservation Biology, 22, 965–975.
- Drummond, A.J., Rambaut, A., Shapiro, B. & Pybus, O.G. (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution, 22, 1185–1192.
- Drummond, A.J., Ashton, B., Cheung, M., Heled, J., Kearse, M., Moir, R., Stones-Havas, S., Thierer, T. & Wilson, A. (2009) Geneious v7.0.6. Available at: http://www.geneious.com/.
- Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969–1973.
- El-Etreby, S.G., Roberts, C.M., Ghobashy, A.A. & Zyadah, M.A. (1993) Coral reef groupers (family: Serranidae) in south Sinai: reproduction and hermaphroditism in the fish Cephalopholis hemistiktos (Rüppell, 1830). Journal of the Egyptian German Society of Zoology (Anatomy and Embryology), 12(B), 1–19.
- Excoffier, L. & Lischer, H.E. (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564–567.
- Excoffier, L., Smouse, P.E. & Quattro, J.M. (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131, 479.
- Feary, D.A., Burt, J.A., Bauman, A.G., Usseglio, P., Sale, P.F. & Cavalcante, G.H. (2010) Fish communities on the world's warmest reefs: what can they tell us about the effects of climate change in the future? Journal of Fish Biology, 77, 1931–1947.
- Fernandez-Silva, I., Randall, J.E., Coleman, R.R., DiBattista, J.D., Rocha, L.A., Reimer, J.D., Meyer, C.G. & Bowen, B.W. (in press) Yellow tails in a Red Sea: phylogeography of the Indo-Pacific goatfish Mulloidichthys flavolineatus reveals isolation in peripheral provinces and cryptic evolutionary lineages. Journal of Biogeography. doi: 10.1111/jbi.12598.
10.1111/jbi.12598 Google Scholar
- Fu, Y.-X. (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147, 915–925.
- Gaines, S.D., White, C., Carr, M.H. & Palumbi, S.R. (2010) Designing marine reserve networks for both conservation and fisheries management. Proceedings of the National Academy of Sciences, 107, 18286–18293.
- 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.
- Giles, E.C., Saenz-Agudelo, P., Hussey, N.E., Ravasi, T. & Berumen, M.L. (2015) Exploring seascape genetics and kinship in the reef sponge Stylissa carteri in the Red Sea. Ecology and Evolution, doi:10.1002/ece3.1511.
- Gladstone, W. (2002) Fisheries of the Farasan Islands (Red Sea). Naga, WorldFish Center Quarterly, 25, 30–34.
- Guindon, S. & Gascuel, O. (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology, 52, 696–704.
- Gust, N., Choat, J.H. & Ackerman, J.L. (2002) Demographic plasticity in tropical reef fishes. Marine Biology, 140, 1039–1051.
- Harpending, H.C. (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biology, 66, 591–600.
- Harrison, H.B., Williamson, D.H., Evans, R.D., Almany, G.R., Thorrold, S.R., Russ, G.R., Feldheim, K.A., van Herwerden, L., Planes, S., Srinivasan, M., Berumen, M.L. & Jones, G.P. (2012) Larval export from marine reserves and the recruitment benefit for fish and fisheries. Current Biology, 22, 1023–1028.
- Harrison, H.B., Saenz-Agudelo, P., Planes, S., Jones, G.P. & Berumen, M.L. (2013) Relative accuracy of three common methods of parentage analysis in natural populations. Molecular Ecology, 22, 1158–1170.
- Hashim, O. (1993) Fisheries study in the Gulf. Marine Pollution Bulletin, 27, 279–284.
- Hastings, A. & Botsford, L.W. (2006) Persistence of spatial populations depends on returning home. Proceedings of the National Academy of Sciences of the USA, 103, 6067–6072.
- Hedgecock, D., Barber, P.H. & Edmands, S. (2007) Genetic approaches to measuring connectivity. Oceanography, 20, 70–79.
- Hellberg, M.E. (2007) Footprints on water: the genetic wake of dispersal among reefs. Coral Reefs, 26, 463–473.
- Hellberg, M.E. (2009) Gene flow and isolation among populations of marine animals. Annual Review of Ecology Evolution and Systematics, 40, 291–310.
- Hixon, M.A., Pacala, S.W. & Sandin, S.A. (2002) Population regulation: historical context and contemporary challenges of open vs. closed systems. Ecology, 83, 1490–1508.
- Jones, G.P., Planes, S. & Thorrold, S.R. (2005) Coral reef fish larvae settle close to home. Current Biology, 15, 1314–1318.
- Kimura, D.K. (1980a) Likelihood methods for the von Bertalanffy growth curve. Fishery Bulletin, 77, 765–774.
- Kimura, M. (1980b) A simple method for estimating evlutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120.
- Kritzer, J.P. (2002) Variation in the population biology of stripey bass Lutjanus carponotatus within and between two island groups on the Great Barrier Reef. Marine Ecology Progress Series, 243, 191–207.
- Kritzer, J.P. & Sale, P.F. (2004) Metapopulation ecology in the sea: from Levins' model to marine ecology and fisheries science. Fish and Fisheries, 5, 131–140.
- Kritzer, J.P., Davies, C.R. & Mapstone, B.D. (2001) Characterizing fish populations: effects of sample size and population structure on the precision of demographic parameter estimates. Canadian Journal of Fisheries and Aquatic Sciences, 58, 1557–1568.
- Leis, J.M. (2002) Pacific coral-reef fishes: the implications of behaviour and ecology of larvae for biodiversity and conservation, and a reassessment of the open population paradigm. Environmental Biology of Fishes, 65, 199–208.
- Lessios, H.A. (2008) The great American schism: divergence of marine organisms after the rise of the Central American Isthmus. Annual Review of Ecology, Evolution, and Systematics, 39, 63–91.
- Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.
- McCormick, M.I. & Molony, B.W. (1995) Influence of water temperature during the larval stage on size, age and body condition of a tropical reef fish at settlement. Marine Ecology Progress Series, 118, 59–68.
- McIlwain, J.L., Claereboudt, M.R., Al-Oufi, H.S., Zaki, S. & Goddard, J.S. (2005) Spatial variation in age and growth of the kingfish (Scomberomorus commerson) in the coastal waters of the Sultanate of Oman. Fisheries Research, 73, 283–298.
- Meeker, N.D., Hutchinson, S.A., Ho, L. & Trede, N.S. (2007) Method for isolation of PCR-ready genomic DNA from zebrafish tissues. BioTechniques, 43, 610–614.
- Messmer, V., van Herwerden, L., Munday, P.L. & Jones, G.P. (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.
- Moritz, C. (1994) Defining ‘evolutionarily significant units’ for conservation. Trends in Ecology and Evolution, 9, 373–375.
- Ormond, R. & Edwards, A. (1987) Red Sea fishes. Key environments – Red Sea (ed. by A.J. Edwards and S.M. Head), pp. 251–287. Pergamon Press, Oxford.
- Pianka, E.R. (1978) Evolutionary ecology. Harper & Row Publishers, New York.
- Rambaut, A., Suchard, M.A., Xie, D. & Drummond, A.J. (2014) Tracer v1.6. Available at: http://beast.bio.ed.ac.uk/Tracer.
- Randall, J.E. (1994) Twenty-two new records of fishes from the Red Sea. Fauna of Saudi Arabia, 14, 259–275.
- Randall, J.E. & Ben-Tuvia, A. (1983) R review of the groupers (Pisces: Serranidae: Epinephelinae) of the Red Sea, with descriptions of a new species of Cephalopholis. Bulletin of Marine Science, 33, 373–426.
- Riginos, C. & Victor, B.C. (2001) Larval spatial distributions and other early life-history characteristics predict genetic differentiation in eastern Pacific blennioid fishes. Proceedings of the Royal Society B: Biological Sciences, 268, 1931–1936.
- Roberts, C.M. & Polunin, N.V.C (1992) Effects of marine reserve protection on northern Red Sea fish populations. Proceedings of the 7th International Coral Reef Symposium, Guam, 2, 969–977.
- Roberts, C.M., Shepherd, A.R.D. & Ormond, R.F.G. (1992) Large-scale variation in assemblage structure of Red Sea butterflyfishes and angelfishes. Journal of Biogeography, 19, 239–250.
- Rocha, L.A. (2004) Mitochondrial DNA and color pattern variation in three Western Atlantic Halichoeres (Labridae), with the revalidation of two species. Copeia, 4, 770–782.
- Rocha, L.A., Bass, A.L., Robertson, D.R. & Bowen, B.W. (2002) Adult habitat preferences, larval dispersal, and the comparative phylogeography of three Atlantic surgeonfishes (Teleostei: Acanthuridae). Molecular Ecology, 11, 243–252.
- Rocha, L.A., Craig, M.T. & Bowen, B.W. (2007) Phylogeography and the conservation of coral reef fishes. Coral Reefs, 26, 501–512.
- Rogers, A.R. & Harpending, H. (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution, 9, 552–569.
- Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.
- Savidge, G., Lennon, J. & Matthews, J. (1990) A shore-based survey of upwelling along the coast of the Dhofar region, southern Oman. Continental Shelf Research, 10, 259–275.
- Schils, T. & Coppejans, E. (2003) Phytogeography of upwelling areas in the Arabian Sea. Journal of Biogeography, 30, 1339–1356.
- Seutin, G., White, B.N. & Boag, P.T. (1991) Preservation of avian blood and tissue samples for 654 DNA analyses. Canadian Journal of Zoology, 69, 82–90.
- Sheppard, C., Price, A. & Roberts, C. (1992) Marine ecology of the arabian region: patterns and processes in extreme tropical environments. Academic Press, Toronto.
- Shpigel, M. & Fishelson, L. (1989) Habitat partitioning between species of the genus Cephalopholis (Pisces, Serranidae) across the fringing reef of the Gulf of Aqaba (Red Sea). Marine Ecology Progress Series, 58, 17–22.
- Siddall, M., Rohling, E.J., Almogi-Labin, A., Hemleben, C., Meischner, D., Schmelzer, I. & Smeed, D.A. (2003) Sea-level fluctuations during the last glacial cycle. Nature, 423, 853–858.
- Simpson, S.D., Harrison, H.B., Claereboudt, M.R. & Planes, S. (2014) Long-distance dispersal via ocean currents connects Omani clownfish populations throughout entire species range. PLoS ONE, 9, e107610.
- Slatkin, M. (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution, 47, 264–279.
- Spaet, J.L.Y., Jabado, R.W., Henderson, A.C., Moore, A.B.M. & Berumen, M.L. (2015) Population genetics of four heavily exploited shark species around the Arabian Peninsula. Ecology and Evolution, doi:10.1002/ece3.1515.
- Sponaugle, S., Grorud-Colvert, K. & Pinkard, D. (2006) Temperature-mediated variation in early life history traits and recruitment success of the coral reef fish Thalassoma bifasciatum in the Florida Keys. Marine Ecology Progress Series, 308, 1–15.
- Stephens, M. & Donnelly, P. (2003) A comparison of bayesian methods for haplotype reconstruction from population genotype data. The American Journal of Human Genetics, 73, 1162–1169.
- Swofford, D.L. (2002) PAUP*: phylogenetic analyses using Parsimony (*and Other Methods), Version 4. Sinauer Associates, Sutherland, MA.
- Tamura, K. & Nei, M. (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10, 512–526.
- Taylor, B.M. & McIlwain, J.L. (2010) Beyond abundance and biomass: effects of marine protected areas on the demography of a highly exploited reef fish. Marine Ecology Progress Series, 411, 243–258.
- Thresher, R.E., Colin, P.L. & Bell, L.J. (1989) Planktonic duration, distribution and population structure of western and central Pacific Damselfishes (Pomacentridae). Copeia, 2, 420–434.
10.2307/1445439 Google Scholar
- Ward, R.D., Zemlak, T.S., Innes, B.H., Last, P.R. & Hebert, P.D. (2005) DNA barcoding Australia's fish species. Philosophical Transactions of the Royal Society B: Biological Sciences, 360, 1847–1857.
- Weersing, K. & Toonen, R.J. (2009) Population genetics, larval dispersal, and connectivity in marine systems. Marine Ecology-Progress Series, 393, 1–12.
- White, C., Selkoe, K.A., Watson, J., Siegel, D.A., Zacherl, D.C. & Toonen, R.J. (2010) Ocean currents help explain population genetic structure. Proceedings of the Royal Society B: Biological Sciences, 277, 1685.
- Whitlock, M.C. & McCauley, D.E. (1999) Indirect measures of gene flow and migration: FST = 1/(4Nm+ 1). Heredity, 82, 117–125.