Phylogeography of the copper shark (Carcharhinus brachyurus) in the southern hemisphere: implications for the conservation of a coastal apex predator
Martin T. Benavides A , Kevin A. Feldheim B , Clinton A. Duffy C , Sabine Wintner D , J. Matias Braccini E , Jessica Boomer F , Charlie Huveneers G H , Paul Rogers G H , Jeffrey C. Mangel I J , Joanna Alfaro-Shigueto I J , Daniel P. Cartamil K and Demian D. Chapman AA Institute for Ocean Conservation Science and School of Marine and Atmospheric Science, Stony Brook University, Stony Brook, New York 11794, USA.
B Field Museum, Pritzker Laboratory for Molecular Systematics and Evolution, 1400 South Lake Shore Drive, Chicago, IL 60605, USA.
C Aquatic and Threats Unit, Department of Conservation, Auckland, New Zealand.
D KwaZulu-Natal Sharks Board, Private Bag 2, Umhlanga Rocks 4320, and Biomedical Resource Unit, University of KwaZulu–Natal, Durban 4000, South Africa.
E Fisheries Centre, The University of British Columbia, Vancouver, BC V6T1Z4, Canada. Present address: Queensland Department of Employment, Economic Development and Innovation, Southern Fisheries Centre, Deception Bay, Qld 4508, Australia.
F Department of Biological Sciences, Macquarie University, NSW 2109, Australia.
G Threatened, Endangered, and Protected Species Subprogram, SARDI – Aquatic Sciences, Adelaide, SA 5024, Australia.
H School of Biological Sciences, Flinders University, Adelaide, SA 5043, Australia.
I Pro Delphinus, Octavio Bernal 572-5, Lima 11, Perú.
J Centre for Ecology and Conservation, School of Biosciences, University of Exeter, Cornwall Campus, Penryn, Cornwall, TR10 9EZ, United Kingdom.
K Scripps Institution of Oceanography, University of California, San Diego, 9500 Gilman Drive (Mail code: 0204), La Jolla, CA 92093-0204, USA.
L Corresponding author. Email: demian.chapman@stonybrook.edu
Marine and Freshwater Research 62(7) 861-869 https://doi.org/10.1071/MF10236
Submitted: 9 September 2011 Accepted: 15 January 2011 Published: 25 July 2011
Abstract
The copper or bronze whaler shark (Carcharhinus brachyurus) is a large, coastal top predator that is vulnerable to overexploitation. We test the null hypothesis that copper sharks are panmictic throughout the southern hemisphere. We analysed part of the mitochondrial control region (mtCR) in 120 individuals from eight sampling areas, defining 20 mtCR haplotypes (h = 0.76 ± 0.06, π = 0.016 ± 0.0007). Significant genetic structure was detected among the following three major coastal regions separated by oceanic habitat: Australia–New Zealand, South Africa–Namibia and Perú (AMOVA ΦST = 0.95, P < 0.000001). A major phylogeographic discontinuity exists across the Indian Ocean, indicating an absence of at least female-mediated gene flow for ~3 million years. We propose that this species originated in the Atlantic, experienced vicariant isolation of Pacific and Atlantic lineages by the rise of the Isthmus of Panama and, subsequently, dispersed across the Pacific to colonise Australasia. Oceanic expanses appear to be traversed over evolutionary but not ecological timescales, which means that regional copper-shark populations should be assessed and managed independently.
Additional keywords: bronze whaler, control region, fin trade, mitochondrial DNA, population genetics.
References
Ahonen, H., Hartcourt, R., and Stow, A. (2009). Nuclear and mitochondrial DNA reveals isolation of imperilled grey nurse shark populations (Carcharias taurus). Molecular Ecology 18, 4409–4421.| Nuclear and mitochondrial DNA reveals isolation of imperilled grey nurse shark populations (Carcharias taurus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFaitrbE&md5=be2d4d6d63fe4b147f544035c133649fCAS |
Castro, A. L. F., Stewart, B. S., Wilson, S. G., Hueter, R. E., Meekan, M. G., Motta, P. J., Bowen, B. W., and Karl, S. A. (2007). Population genetic structure of Earth’s largest fish, the whale shark (Rhincodon typus). Molecular Ecology 16, 5183–5192.
| Population genetic structure of Earth’s largest fish, the whale shark (Rhincodon typus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVGmsrY%3D&md5=c41d63efd90a30115820d167aa822c6eCAS |
Cavanagh, R. D., Kyne, P. M., Fowler, S., Musick, J. A., and Benett, M. B. (2003). ‘Conservation Status of Australasian Chondrichthyans.’ IUCN Shark Specialist Group. Australia and Oceania Regional Red List Workshop, 7–9 March 2003, Brisbane.
Chabot, C. L., and Allen, L. G. (2009). Global population structure of the tope (Galeorhinus galeus) inferred by mitochondrial control region sequence data. Molecular Ecology 18, 545–552.
| Global population structure of the tope (Galeorhinus galeus) inferred by mitochondrial control region sequence data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsVKls7g%3D&md5=a7a452cd801dc14a537ac7f5b510f606CAS |
Chapman, D. D., Pinhal, D., and Shivji, M. S. (2009). Tracking the fin trade: genetic stock identification in western Atlantic scalloped hammerhead sharks Sphyrna lewini. Endangered Species Research 9, 221–228.
| Tracking the fin trade: genetic stock identification in western Atlantic scalloped hammerhead sharks Sphyrna lewini.Crossref | GoogleScholarGoogle Scholar |
Clarke, S., Magnussen, J. E., Abercrombie, D. L., McAllister, M. K., and Shivji, M. S. (2006). Identification of shark species composition and proportion in the Hong Kong fin market based on molecular genetics and trade records. Conservation Biology 20, 201–211.
| Identification of shark species composition and proportion in the Hong Kong fin market based on molecular genetics and trade records.Crossref | GoogleScholarGoogle Scholar |
Clement, M., Posada, D., and Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.
| TCS: a computer program to estimate gene genealogies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnvV2gtbw%3D&md5=8b0fd9917aeeaf3d556b8addd7601149CAS |
Cliff, G., and Dudley, S. F. J. (1992). Sharks caught in the protective beach nets of South Africa. 6. The copper shark Carcharhinus brachyurus (Gunther). South African Journal of Marine Science-Suid-Afrikaanse Tydskrif Vir Seewetenskap 12, 663–674.
Compagno, L., Dando, M., and Fowler, S. (2005). ‘Sharks of the World.’ (Princeton University Press: Princeton, NJ.)
Dudgeon, C. L., Broderick, D., and 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.
| IUCN classification zones concord with, but underestimate, the population genetic structure of the zebra shark Stegostoma fasciatum in the Indo-West Pacific.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivVGktb8%3D&md5=3f1e91a6bf59a93d1f8ac10c50212798CAS |
Duffy, C., and Gordon, I. (2003). Carcharhinus brachyurus. In ‘IUCN 2009. IUCN Red List of Threatened Species. Version 2009.1’. Available at www.iucnredlist.org [accessed 9 July 2009].
Duncan, K. M., Martin, A. P., Bowen, B. W., and De Couet, H. G. (2006). Global phylogeography of the scalloped hammerhead shark (Sphyrna lewini). Molecular Ecology 15, 2239–2251.
| Global phylogeography of the scalloped hammerhead shark (Sphyrna lewini).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xot1ait70%3D&md5=7d11982f055e959e3bc6fb72fbd483b3CAS |
Excoffier, L., Smouse, P. E., and Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491.
| 1:CAS:528:DyaK38XlsVCntro%3D&md5=9f6541d7bfa334476aff4e812ac709cfCAS |
Feldheim, K. A., Gruber, S. H., and Ashley, M. V. (2004). Reconstruction of parental microsatellite genotypes reveals female polyandry and philopatry in the lemon shark, Negaprion brevirostris. Evolution 58, 2332–2342.
| 1:CAS:528:DC%2BD2cXhtVentLnL&md5=21358a1bccc0a1e7c045e65e5782bc15CAS |
Garrick, J. A. F. (1982). Sharks of the genus Carcharhinus. NOAA Technical Report NMFS Circular 445. National Oceanic and Atmospheric Administration, Silver Springs, MD.
Heim, B., and Bourdon, J. (1998). Fossil species: Carcharhinus brachyurus. In ‘The Life and Times of Long Dead Sharks’. Available at http://www.elasmo.com/frameMe.html?file=genera/cenozoic/species/c_brachyurus.htmlandmenu=bin/menu_genera-alt.html [accessed 21 July 2010].
Keeney, D. B., and 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.
| Worldwide phylogeography of the blacktip shark (Carcharhinus limbatus) inferred from mitochondrial DNA reveals isolation of western Atlantic populations coupled with recent Pacific dispersal.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1OisL%2FJ&md5=e2d964d00145929986a9f20209975e7bCAS |
Keeney, D. B., Heupel, M., Hueter, R. E., and Heist, E. J. (2003). Genetic heterogeneity among blacktip shark, Carcharhinus limbatus, continental nurseries along the US Atlantic and Gulf of Mexico. Marine Biology 143, 1039–1046.
| Genetic heterogeneity among blacktip shark, Carcharhinus limbatus, continental nurseries along the US Atlantic and Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |
Last, P. R., and Stevens, J. D. (2009). ‘Sharks and Rays of Australia.’ (CSIRO Publishing: Melbourne.)
Long, D. J. (1993). Preliminary list of the marine fishes and other vertebrate remains from the late Pleistocene Palos Verdes sand formation at Costa Mesa, Orange County, California. PaleoBios 15, 9–13.
Lucifora, L. O., Menni, R. C., and Escalante, A. H. (2005). Reproduction and seasonal occurence of the copper shark, Carcharhinus brachyurus, from north Patagonia, Argentina. ICES Journal of Marine Science 62, 107–115.
| Reproduction and seasonal occurence of the copper shark, Carcharhinus brachyurus, from north Patagonia, Argentina.Crossref | GoogleScholarGoogle Scholar |
Marsili, S. (2008). Systematic, paleoecologic and paleobiogeographic analysis of the Plio–Pleistocene Mediterranean elasmobranch fauna. Atti Della Società Toscana Di Scienze Naturali Memorie Serie A 113, 81–88.
Moritz, C. (1994). Applications of mitochondrial DNA analysis in conservation: a critical review. Molecular Ecology Notes 3, 401–411.
| 1:CAS:528:DyaK2MXhtlyktrw%3D&md5=22753ab7ee99501b9d085e87bc34f5f3CAS |
Nielsen, R., and Wakeley, J. (2001). Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 158, 885–896.
| 1:CAS:528:DC%2BD3MXltFSisbg%3D&md5=eb8d548d6c88df3d4bc9ac4fee451354CAS |
Pardini, A. T., Jones, C. S., Noble, L. R., Kreiser, B., Malcolm, H., Bruce, B. D., Stevens, J. D., Cliff, G., Scholl, M. C., Francis, M., Duffy, C. A. J., and Martin, A. P. (2001). Sex-biased dispersal of great white sharks. Nature 412, 139–140.
| Sex-biased dispersal of great white sharks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsFWnsr4%3D&md5=3bcf499d9706ee72315bc42cd06bd219CAS |
Portnoy, D., McDowell, J., Heist, E., Musick, J., and Graves, J. (2010). World phylogeography and male-mediated gene flow in the sandbar shark, Carcharhinus plumbeus. Molecular Ecology 19, 1994–2010.
| World phylogeography and male-mediated gene flow in the sandbar shark, Carcharhinus plumbeus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnsl2jsb4%3D&md5=eebce8bd8e886297494e50d4d52627e4CAS |
Posada, D. (2008). jModeltest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.
| jModeltest: phylogenetic model averaging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotlKgsb4%3D&md5=8204418ef76c37579475b5dca5cf0565CAS |
Rozas, J., Sánchez-DelBarrio, J. C., Messeguer, X., and Rozas, R. (2003). DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497.
| DnaSP, DNA polymorphism analyses by the coalescent and other methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvVSisLo%3D&md5=0169a23eacc4a1663959dbdbae60c17bCAS |
Schneider, S., Roessli, D., and Excoffer, L. (2000). ‘ARLEQUIN ver. 2.000. A Software for Population Genetics Data Analysis.’ (Genetics and Biometry Laboratory, Department of Anthropology and Ecology, University of Geneva: Geneva.)
Schultz, J. K., Feldheim, K. A., Gruber, S. H., Ashley, M. V., McGovern, T. M., and Bowen, B. W. (2008). Global phylogeography and seascape genetics of the lemon sharks (genus Negaprion). Molecular Ecology 17, 5336–5348.
| Global phylogeography and seascape genetics of the lemon sharks (genus Negaprion).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M%2FltVyluw%3D%3D&md5=ece5a94bf182b4be84d5c74c639637d8CAS |
Smith, S. E., Au, D. W., and Show, C. (1998). Intrinsic rebound potentials of 26 species of Pacific sharks. Marine and Freshwater Research 49, 663–678.
| Intrinsic rebound potentials of 26 species of Pacific sharks.Crossref | GoogleScholarGoogle Scholar |
Stow, A., Zenger, K., Briscoe, D., Gillings, M., Peddemors, V., Otway, N., and Harcourt, R. (2006). Isolation and genetic diversity of endangered grey nurse (Carcharias taurus) populations. Biology Letters 2, 308–311.
| Isolation and genetic diversity of endangered grey nurse (Carcharias taurus) populations.Crossref | GoogleScholarGoogle Scholar |
Walter, J. P., and Ebert, D. A. (1991). Preliminary estimates of age in the bronze whaler, Carcharhinus brachyurus (Chondrichthyes, Carcharhinidae) from southern Africa, with a review of some life history parameters. South African Journal of Marine Science–Suid-Afrikaanse Tydskrif Vir Seewetenskap 10, 37–44.