Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Genetic population structure and connectivity in a commercially exploited and wide-ranging deepwater shark, the leafscale gulper (Centrophorus squamosus)

A. Veríssimo A B , J. R. McDowell A and J. E. Graves A
+ Author Affiliations
- Author Affiliations

A Virginia Institute of Marine Science, College of William & Mary, PO Box 1346, Gloucester Point, VA 23062, USA.

B Corresponding author. Email: averissimo@vims.edu

Marine and Freshwater Research 63(6) 505-512 https://doi.org/10.1071/MF11237
Submitted: 28 October 2011  Accepted: 6 March 2012   Published: 13 June 2012

Abstract

The leafscale gulper (Centrophorus squamosus) is a wide-ranging deepwater benthopelagic shark threatened by commercial fisheries in parts of its range. Despite concerns about resource sustainability, little is known about the population structure and connectivity between critical habitats of the leafscale gulper. This study investigates the genetic population structure and the migration patterns of C. squamosus using nuclear microsatellites and mitochondrial NADH dehydrogenase subunit 2 (ND2) gene sequences. Genetic diversity was estimated and compared among sample collections from off Ireland, Portugal, the Azores, South Africa and New Zealand. The null hypothesis of genetic homogeneity among all collections was not rejected by the nuclear loci (FST (the overall genetic differentiation among sample collections) = –0.002, P = 0.88), but we found long-term genetic divergence between New Zealand and the remaining collections at the mtDNA ND2 (FCT (genetic differentation among groups of sample collections) = 0.366, P = 0.000). Migration rate estimates indicated limited female dispersal across the Indian Ocean whereas males showed less restricted dispersal. Our results are consistent with a single genetic stock of C. squamosus and the existence of sex-biased dispersal across the Indian Ocean. Widespread genetic homogeneity at nuclear loci minimizes the loss of unique adaptive genetic diversity in the event of localised depletion. However, high local fishing mortality may have far reaching impacts given the marked sex- and maturity-stage-based habitat partitioning previously reported for C. squamosus.

Additional keywords: elasmobranch, top-predator.


References

Allendorf, F. W., and Luikart, G. (2007). ‘Conservation and the Genetics of Populations.’ (Blackwell Publishing Ltd: Padstow.)

Bandelt, H.-J., Forster, P., and Röhl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.
| 1:CAS:528:DyaK1MXjvVGltA%3D%3D&md5=5492935ca830fddd24f946ecc1439725CAS |

Bañón, R., Piñero, C., and Casas, M. (2006). Biological aspects of deep-water sharks Centroscymnus coelolepis and Centrophorus squamosus in Galician waters (north-western Spain). Journal of the Marine Biological Association of the United Kingdom 86, 843–846.
Biological aspects of deep-water sharks Centroscymnus coelolepis and Centrophorus squamosus in Galician waters (north-western Spain).Crossref | GoogleScholarGoogle Scholar |

Beerli, P. (1998). Estimation of migration rates and population sizes in geographically structured populations. In ‘Advances in Molecular Ecology’. (Ed. G. Carvalho.) pp. 39–53. (IOS Press: Amsterdam.)

Beerli, P., and Felsenstein, J. (1999). Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 152, 763–777.
| 1:STN:280:DyaK1M3ot1Gitg%3D%3D&md5=88b7621c7c452694dc3717a5d666a28eCAS |

Beerli, P., and Felsenstein, J. (2001). Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proceedings of the National Academy of Sciences of the United States of America 98, 4563–4568.
Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtVagtLY%3D&md5=ef2d2239569c567ffe531efbc92ebce1CAS |

Chevolot, M., Wolfs, P. H. J., Pálsson, J., Rijnsdorp, A. D., Stam, W. T., and Olsen, J. L. (2007). Population structure and historical demography of the thorny skate (Amblyraja radiata, Rajidae) in the North Atlantic. Marine Biology 151, 1275–1286.
Population structure and historical demography of the thorny skate (Amblyraja radiata, Rajidae) in the North Atlantic.Crossref | GoogleScholarGoogle Scholar |

Clarke, M. W., Conolly, P. L., and Bracken, J. J. (2001a). Aspects of the reproduction of the deep water sharks Centroscymnus coelolepis and Centrophorus squamosus from west of Ireland and Scotland. Journal of the Marine Biological Association of the United Kingdom 81, 1019–1029.
Aspects of the reproduction of the deep water sharks Centroscymnus coelolepis and Centrophorus squamosus from west of Ireland and Scotland.Crossref | GoogleScholarGoogle Scholar |

Clarke, M. W., Conolly, P. L., and Bracken, J. J. (2001b). Biology of exploited deep-water sharks West of Ireland and Scotland. North Atlantic Fisheries Organization Scientific Council Report Doc. 01/108, 18 pp. Available at archive.nafo.int/open/sc/2001/scr01–108.pdf [accessed 13 December 2011].

Clarke, M. W., Conolly, P. L., and Bracken, J. J. (2002). Age estimation of the exploited deepwater shark Centrophorus squamosus from the continental slopes of the Rockall Through and Porcupine Bank. Journal of Fish Biology 60, 501–514.
Age estimation of the exploited deepwater shark Centrophorus squamosus from the continental slopes of the Rockall Through and Porcupine Bank.Crossref | GoogleScholarGoogle Scholar |

Compagno, L. J. V., Dando, M., and Fowler, S. (2005). ‘Sharks of the World.’ (Princeton University Press: Princeton, NJ.)

Crawford, N. G. (2010). SMOGD: software for the measurement of genetic diversity. Molecular Ecology Resources 10, 556–557.
SMOGD: software for the measurement of genetic diversity.Crossref | GoogleScholarGoogle Scholar |

Ellegren, H. (2000). Microsatellite mutations in the germline: implications for evolutionary inference. Trends in Genetics 16, 551–558.
Microsatellite mutations in the germline: implications for evolutionary inference.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotlCnt70%3D&md5=a4468200aa015f0139d9076628a62b40CAS |

Excoffier, L., and Lischer, H. E. L. (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.
Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows.Crossref | GoogleScholarGoogle Scholar |

Excoffier, L., Smouse, P., and Quattro, J. (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=9c0640beefdd6f7f3c14397c8117bf33CAS |

Figueiredo, I., Moura, T., Neves, A., and Gordo, L. S. (2008). Reproductive strategy of leafscale gulper shark Centrophorus squamosus and the Portuguese dogfish Centroscymnus coelolepis on the Portuguese continental slope. Journal of Fish Biology 73, 206–225.
Reproductive strategy of leafscale gulper shark Centrophorus squamosus and the Portuguese dogfish Centroscymnus coelolepis on the Portuguese continental slope.Crossref | GoogleScholarGoogle Scholar |

García, V. B., Lucifora, L. O., and Myers, R. A. (2008). The importance of habitat and life history to extinction risk in sharks, skates, rays and chimaeras. Proceedings. Biological Sciences 275, 83–89.
The importance of habitat and life history to extinction risk in sharks, skates, rays and chimaeras.Crossref | GoogleScholarGoogle Scholar |

Glenn, T. C., and Schable, N. A. (2005). Isolating microsatellite DNA loci. Methods in Enzymology 395, 202–222.
Isolating microsatellite DNA loci.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotlGrtb4%3D&md5=ff854da9d2ac34533b5df15c971b9f4cCAS |

Goudet, J. (2002). ‘FSTAT, a program to estimate and test gene diversities and fixation indices (ver. 2.9.3.2).’ Available at http://www2.unil.ch/popgen/softwares/fstat.htm. [Accessed 14 March 2011].

Graham, K. J., Andrew, N. L., and Hodgson, K. E. (2001). Changes in relative abundance of sharks and rays on Australian South East fishery trawl grounds after twenty years of fishing. Marine and Freshwater Research 52, 549–561.
Changes in relative abundance of sharks and rays on Australian South East fishery trawl grounds after twenty years of fishing.Crossref | GoogleScholarGoogle Scholar |

Griffiths, A. M., Sims, D. W., Johnson, A., Lynghammar, A., McHugh, M., Bakken, T., and Genner, M. J. (2011). Levels of connectivity between longnose skate (Dipturus oxyrinchus) in the Mediterranean Sea and the north-eastern Atlantic Ocean. Conservation Genetics 12, 577–582.
Levels of connectivity between longnose skate (Dipturus oxyrinchus) in the Mediterranean Sea and the north-eastern Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar |

Hasegawa, M., Kishino, H., and Yano, T. (1985). Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22, 160–174.
Dating of the human-ape splitting by a molecular clock of mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXmtFSns7g%3D&md5=13652ae4a1825cc07d3f924c8c4e6191CAS |

Heist, E. (2004) Genetics of sharks, skates and rays. In ‘Biology of Sharks and their Relatives’. (Eds J. C. Carrier, J. A. Musick and M. R. Heithaus.) pp. 471–485. (CRC Press: Boca Raton, FL.)

ICES (2010). Report of the Working Group on Elasmobranch Fishes (WGEF), 22–29 June 2010, Horta, Portugal. ICES CM 2010/ACOM:19. Available at http://www.ices.dk/workinggroups/ViewWorkingGroup.aspx?ID=123 [accessed 1 November 2010]

Jost, L. (2008). Gst and its relatives do not measure differentiation. Molecular Ecology 17, 4015–4026.
Gst and its relatives do not measure differentiation.Crossref | GoogleScholarGoogle Scholar |

Kyne, P. M., and Simpfendorfer, C. A. (2010). Deepwater chondrichthyans. In ‘Sharks and Their Relatives II – Biodiversity, Adaptive Physiology and Conservation’. (Eds J. C. Carrier, J. A. Musick and M. R. Heithaus.) pp. 37–113. (CRC Press: Boca Raton, FL.)

Last, P., and Stevens, J. D. (2009). ‘Sharks and Rays of Australia.’ (Harvard University Press: Melbourne.)

Librado, P., and Rozas, J. (2009). DnaSP ver. 5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.
DnaSP ver. 5: a software for comprehensive analysis of DNA polymorphism data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtFeqtr8%3D&md5=8ec9364da447684c6d55141ff6879eb4CAS |

Martin, A. P. (1999). Substitution rates of organelle and nuclear genes in sharks: implicating metabolic rate (again). Molecular Biology and Evolution 16, 996–1002.
| 1:CAS:528:DyaK1MXksFOlsLw%3D&md5=dc3261e31ddf87f37a6f12de1930c97cCAS |

Martin, A. P., and Palumbi, S. R. (1993). Body size, metabolic rate, generation time, and molecular clock. Proceedings of the National Academy of Sciences of the USA 90, 4087–4091.
| 1:CAS:528:DyaK3sXkt1ehs7o%3D&md5=0e5c156a99642d3483a03a6d366c061dCAS |

Martin, A. P., Naylor, G. J. P., and Palumbi, S. R. (1992). Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Nature 357, 153–155.
Rates of mitochondrial DNA evolution in sharks are slow compared with mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XktVCmtLg%3D&md5=4a87477e096f3fb234a390bb5968cefdCAS |

Morato, T., Watson, R., Pitcher, T. J., and Pauly, D. (2006). Fishing down the deep. Fish and Fisheries 7, 24–34.
Fishing down the deep.Crossref | GoogleScholarGoogle Scholar |

Musick, J. A., Harbin, M. M., and Compagno, L. J. V. (2004). Historical zoogeography of the Selachii. In ‘Biology of Sharks and their Relatives’. (Eds J. C. Carrier, J. A. Musick and M. R. Heithaus.) pp. 33–78. (CRC Press: Boca Raton, FL.)

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=e73040bac632a9c2ae2582534b9d9696CAS |

Pajuelo, J. G., González, J. A., and Santana, J. I. (2010). Bycatch and incidental catch of the black scabbardfish (Aphanopus carbo) fishery off the Canary Islands. Fisheries Research 106, 448–453.
Bycatch and incidental catch of the black scabbardfish (Aphanopus carbo) fishery off the Canary Islands.Crossref | GoogleScholarGoogle Scholar |

Polzin, T., and Daneschmand, S. V. (2003). On Steiner trees and minimum spanning trees in hypergraphs. Operations Research Letters 31, 12–20.
On Steiner trees and minimum spanning trees in hypergraphs.Crossref | GoogleScholarGoogle Scholar |

Portnoy, D. S. (2010). Molecular insights into elasmobranch reproductive behavior for conservation and management. In ‘Sharks and Their Relatives II – Biodoversity, Adaptive Physiology and Conservation’. (Eds J. C. Carrier, J. A. Musick and M. R. Heithaus.) pp. 435–457. (CRC Press: Boca Raton, FL.)

Portnoy, D. S., McDowell, J., Heist, E. J., Musick, J. A., and Graves, J. E. (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=fd30cd7dbfb6168ec4be162e7d879112CAS |

Prugnolle, F., and de Meeus, T. (2002). Inferring sex-biased dispersal from population genetic tools: a review. Heredity 88, 161–165.
Inferring sex-biased dispersal from population genetic tools: a review.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD387oslGluw%3D%3D&md5=426370e01c342fa5af50229c8dab83a3CAS |

Raymound, M., and Rousset, F. (1995). Genepop (version 1.2): population genetics software for exact tests and ecumenicism. Heredity 86, 248–249.

Rousset, F. (2008). Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Molecular Ecology Resources 8, 103–106.
Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux.Crossref | GoogleScholarGoogle Scholar |

Rozen, S., and Skaletsky, H. (2000). Primer3 on the WWW for general users and for biologist programmers. Methods in Molecular Biology 132, 365–386.
| 1:CAS:528:DyaK1MXmslKqsbo%3D&md5=a164454bcecf4e3578d7336d61f7d151CAS |

Schmidt, J. V., Schmidt, C. L., Ozer, F., Ernst, R. E., Feldheim, K. A., Ashley, M. V., and Levine, M. (2009). Low genetic differentiation across three major ocean populations of the whale shark, Rhincodon typus. PLoS ONE 4, e4988.
Low genetic differentiation across three major ocean populations of the whale shark, Rhincodon typus.Crossref | GoogleScholarGoogle Scholar |

Schrey, A. W., and 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.
Microsatellite analysis of population structure in the shortfin mako (Isurus oxyrinchus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnt1Gitr4%3D&md5=016ce57f91da49bb64a1b8392864d299CAS |

Seutin, G., White, B. N., and Boag, P. T. (1991). Preservation of avian blood and tissue samples for DNA analyses. Canadian Journal of Zoology 69, 82–90.
Preservation of avian blood and tissue samples for DNA analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlslylur4%3D&md5=b82d939b65ff05eee8f63a80a412d1a8CAS |

Severino, R. B., Afonso-Dias, I., Delgado, J., and Afonso-Dias, M. (2009). Aspects of the biology of the leafscale gulper shark Centrophorus squamosus (Bonnaterre, 1788) off Madeira archipelago. Arquipélago 26, 57–61.

Simpfendorfer, C. A., and Kyne, P. M. (2009). Limited potential to recover from overfishing raises concerns for deep-sea sharks, skates and chimaeras. Environmental Conservation 36, 97–103.
Limited potential to recover from overfishing raises concerns for deep-sea sharks, skates and chimaeras.Crossref | GoogleScholarGoogle Scholar |

Straube, N., Kriwet, J., and Schiewen, U. K. (2011). Cryptic diversity and species assignment of large lantern sharks of the Etmopterus spinax clade from the Southern Hemisphere (Squaliformes, Etmopteridae). Zoologica Scripta 40, 61–75.
Cryptic diversity and species assignment of large lantern sharks of the Etmopterus spinax clade from the Southern Hemisphere (Squaliformes, Etmopteridae).Crossref | GoogleScholarGoogle Scholar |

Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.
| 1:CAS:528:DyaK2MXitlSgu74%3D&md5=21ef800f00164adb8760c4d4d5adffe1CAS |

van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M., and Shipley, P. (2004). MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535–538.
MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvFOktb8%3D&md5=6f597b06f2f24b0b34ab29213daf15c4CAS |

Veríssimo, A., McDowell, J. R., and Graves, J. E. (2011). Population structure of a deep-water squaloid shark, the Portuguese dogfish (Centroscymnus coelolepis). ICES Journal of Marine Science 68, 555–563.
Population structure of a deep-water squaloid shark, the Portuguese dogfish (Centroscymnus coelolepis).Crossref | GoogleScholarGoogle Scholar |

Waples, R. S. (1998). Separating the wheat from the chaff: pattern of genetic differentiation in high gene flow species. The Journal of Heredity 89, 438–450.
Separating the wheat from the chaff: pattern of genetic differentiation in high gene flow species.Crossref | GoogleScholarGoogle Scholar |

Waples, R. S., and Gagggiotti, O. (2006). What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Molecular Ecology 15, 1419–1439.
What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlsVCjur4%3D&md5=23a42e642e58d1f675ccae779adb3eefCAS |