Genomic population structure of great hammerhead sharks (Sphyrna mokarran) across the Indo-Pacific

Naomi L. Brunjes; Samuel M. Williams; Alexis L. Levengood; Matt K. Broadhurst; Vincent Raoult; Alastair V. Harry; Matias Braccini; Madeline E. Green; Julia L. Y. Spaet; Michael J. Travers; Bonnie J. Holmes

doi:10.1071/MF23236

RESEARCH ARTICLE (Open Access)

Previous Next Contents Vol 75(6)

Genomic population structure of great hammerhead sharks (Sphyrna mokarran) across the Indo-Pacific

Naomi L. Brunjes

^A ^* , Samuel M. Williams

^A ^B ^C , Alexis L. Levengood ^A , Matt K. Broadhurst ^C ^D , Vincent Raoult

^E , Alastair V. Harry ^F , Matias Braccini ^F , Madeline E. Green

^G , Julia L. Y. Spaet

^H , Michael J. Travers ^F and Bonnie J. Holmes ^A

+ Author Affiliations

- Author Affiliations

^A University of the Sunshine Coast, School of Science, Technology and Engineering, Sippy Downs, Qld 4556, Australia.

^B Department of Agriculture and Fisheries, Agri-Science Queensland, Dutton Park, Qld 4102, Australia.

^C School of the Environment, The University of Queensland, St Lucia, Qld 4067, Australia.

^D New South Wales Department of Primary Industries and Fisheries, Coffs Harbour, NSW 2450, Australia.

^E Marine Ecology Group, School of Natural Sciences, Macquarie University, Ourimbah, NSW 2109, Australia.

^F Western Australian Fisheries and Marine Research Laboratories, Department of Primary Industries and Regional Development, Government of Western Australia, North Beach, WA 6920, Australia.

^G Institute for Marine and Antarctic Studies, University of Tasmania, Private Bag 49, Hobart, Tas., Australia.

^H Evolutionary Ecology Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UK.

^* Correspondence to: naomibrunjes@gmail.com

Handling Editor: Bradley Wetherbee

Marine and Freshwater Research 75, MF23236 https://doi.org/10.1071/MF23236

Submitted: 22 November 2023 Accepted: 28 February 2024 Published: 10 April 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context

Currently, little information exists describing the population structure of great hammerhead sharks (Sphyrna mokarran) in Australian waters.

Aims

This study used single nucleotide polymorphisms to investigate fine-scale population structure in S. mokarran across the Indo-Pacific.

Methods

DNA was extracted from 235 individuals across six Australian locations and a Red Sea outgroup. Population parameters were calculated and visualised to test structuring across locations.

Key results

No fine-scale population structuring was observed for S. mokarran across the Indo-Pacific. However, population structuring occurred for all Australian locations when compared to the Red Sea outgroup.

Conclusions

Findings suggest a single stock is most likely for S. mokarran found in Australian waters. Results provide key information for understanding the broad range movements of S. mokarran and help to define the scale of management required to preserve genetic diversity in this species. The structuring between Australia and the Red Sea indicates limited gene flow and movement.

Implications

Results indicate that large-scale movements of S. mokarran could be occurring to facilitate genetic mixing. Future research focusing on individual tagging to corroborate movements would be highly beneficial to determine how far (and often) individuals are dispersing, and to note where cross-jurisdictional management, including from neighbouring regions in the Indo-West Pacific–Oceania region, are most critical.

Keywords: Australia, gene flow, management scale, panmixia, population genomics, Red Sea, shark fisheries, single nucleotide polymorphisms.

References

Begg GA, Friedland KD, Pearce JB (1999) Stock identification and its role in stock assessment and fisheries management: an overview. Fisheries Research 43, 1-8.
| Crossref | Google Scholar |

Benestan L (2020) Population genomics applied to fishery management and conservation. In ‘Population Genomics: Marine Organisms’. (Eds MF Oleksiak, OP Rajora) pp. 399–421. (Springer International Publishing: Cham, Switzerland) doi:10.1007/13836_2019_66

Boube T, Azam C-S, Guilbert A, Huveneers C, Papastamatiou YP, Mourier J, Trujillo JE, Femmami N, Kunovsky A, Bersani F, Laurent E, Bousseyroux A, Thellier T, Follin Y, Pavy T, Jeandel V, Mataarere A, Burlot M, Bouyeure J, Rigoreau B, Rigoreau L, Lenormand A, Chalabi F, Hayek M, Jeandel J-M, Stenger P-L (2023) First insights into the population characteristics and seasonal occurrence of the great hammerhead shark, Sphyrna mokarran (Rüppell, 1837) in the Western Tuamotu archipelago, French Polynesia. Frontiers in Marine Science 10, 1234059.
| Crossref | Google Scholar |

Briggs JC (1995) ‘Global biogeography.’ (Elsevier: Arnoldsville, GA, USA)

Broadhurst M, Cullis B (2020) Mitigating the discard mortality of non-target, threatened elasmobranchs in bather-protection gillnets. Fisheries Research 222, 105435.
| Crossref | Google Scholar |

Cardeñosa D, Shea SK, Zhang H, Fischer GA, Simpfendorfer CA, Chapman DD (2022) Two thirds of species in a global shark fin trade hub are threatened with extinction: conservation potential of international trade regulations for coastal sharks. Conservation Letters 15, e12910.
| Crossref | Google Scholar |

Caye K, Deist TM, Martins H, Michel O, Francois O (2016) TESS3: fast inference of spatial population structure and genome scans for selection. Molecular Ecology Resources 16, 540-548.
| Crossref | Google Scholar | PubMed |

Chapman DD, Gruber SH (2002) A further observation of the prey-handling behavior of the great hammerhead shark, Sphyrna mokarran: predation upon the spotted eagle ray, Aetobatus narinari. Bulletin of Marine Science 70, 947-952.
| Google Scholar |

Chapman DD, Feldheim KA, Papastamatiou YP, Hueter RE (2015) There and back again: a review of residency and return migrations in sharks, with implications for population structure and management. Annual Review of Marine Science 7, 547-570.
| Crossref | Google Scholar | PubMed |

Chin A, Simpfendorfer CA, White WT, Johnson GJ, McAuley RB, Heupel MR (2017) Crossing lines: a multidisciplinary framework for assessing connectivity of hammerhead sharks across jurisdictional boundaries. Scientific Reports 7, e46061.
| Crossref | Google Scholar |

Clarke SC, McAllister MK, Milner-Gulland EJ, Kirkwood GP, Michielsens CGJ, Agnew DJ, Pikitch EK, Nakano H, Shivji MS (2006) Global estimates of shark catches using trade records from commercial markets. Ecology Letters 9, 1115-1126.
| Crossref | Google Scholar | PubMed |

Compagno LJV (1984) Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Part 2: Carcharhiniformes. FAO Fish Synopsis 4, pp. 251–655. (Food and Agriculture Organization of the United Nations: Rome, Italy) Available at https://www.fao.org/3/ad123e/ad123e00.htm

Compagno L, Dando M, Fowler S (2005) ‘A field guide to the sharks of the world.’ (Harper-Collins Ltd: London, UK)

Daly-Engel TS, Seraphin KD, Holland KN, Coffey JP, Nance HA, Toonen RJ, Bowen BW (2012) Global phylogeography with mixed-marker analysis reveals male-mediated dispersal in the endangered scalloped hammerhead shark (Sphyrna lewini). PLoS ONE 7, e29986.
| Crossref | Google Scholar | PubMed |

Department of Agriculture, Water and the Environment (2014) Non-detriment finding for the export of shark species listed in the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) and harvested from Australian waters. DAWE, Brisbane, Qld, Australia.

Department of Agriculture Water and the Environment (2021) Fisheries and the environment: Environment Protection and Biodiversity Conservation Act 1999. (DAWE) Available at https://www.dcceew.gov.au/environment/marine/fisheries [Verified 25 May 2022]

Doan MD, Kajiura SM (2020) Adult blacktip sharks (Carcharhinus limbatus) use shallow water as a refuge from great hammerheads (Sphyrna mokarran). Journal of Fish Biology 96, 1530-1533.
| Crossref | Google Scholar | PubMed |

Dudgeon CL, Broderick D, Ovenden JR (2009) IUCN classification zones concord with, but underestimate, the population genetic structure of the zebra shark Stegostoma fasciatum in the Indo-West Pacifc. Molecular Ecology 18, 248-261.
| Crossref | Google Scholar | PubMed |

Dudgeon CL, Blower DC, Broderick D, Giles JL, Holmes BJ, Kashiwagi T, Krück NC, Morgan JAT, Tillett BJ, Ovenden JR (2012) A review of the application of molecular genetics for fisheries management and conservation of sharks and rays. Journal of Fish Biology 80, 1789-1843.
| Crossref | Google Scholar | PubMed |

Dudley SFJ, Simpfendorfer CA (2006) Population status of 14 shark species caught in the protective gillnets off KwaZulu–Natal beaches, South Africa, 1978–2003. Marine and Freshwater Research 57, 225-240.
| Crossref | Google Scholar |

Dulvy NK, Pacoureau N, Rigby CL, Pollom RA, Jabado RW, Ebert DA, Finucci B, Pollock CM, Cheok J, Derrick DH, Herman KB, Sherman CS, VanderWright WJ, Lawson JM, Walls RHL, Carlson JK, Charvet P, Bineesh KK, Fernando D, Ralph GM, Matsushiba JH, Hilton-Taylor C, Fordham SV, Simpfendorfer CA (2021) Overfishing drives over one-third of all sharks and rays toward a global extinction crisis. Current Biology 31, 4773-4787.e8.
| Crossref | Google Scholar | PubMed |

Feldheim KA, Gruber SH, Ashley MV (2001) Multiple paternity of a lemon shark litter (chondrichthyes: Carcharhinidae). Copeia 2001, 781-786.
| Crossref | Google Scholar |

Frankham R, Briscoe DA, Ballou JD (2002) ‘Introduction to conservation genetics’, 2nd edn. (Cambridge University Press: Cambridge, UK)

Frichot E, Francois O (2015) LEA: an R package for landscape and ecological association studies. Methods in Ecology and Evolution 6, 925-929.
| Crossref | Google Scholar |

Gallagher AJ, Hammerschlag N, Shiffman DS, Giery ST (2014) Evolved for extinction: the cost and conservation implications of specialization in hammerhead sharks. BioScience 64, 619-624.
| Crossref | Google Scholar |

Georges A, Gruber B, Pauly GB, White D, Adams M, Young MJ, Kilian A, Zhang X, Shaffer HB, Unmack PJ (2018) Genomewide SNP markers breathe new life into phylogeography and species delimitation for the problematic short-necked turtles (chelidae: Emydura) of eastern Australia. Molecular ecology 27, 5195-5213.
| Crossref | Google Scholar | PubMed |

Gonzalez C, Hammerschlag N, Gallagher A, Caballero S (2017) Population genetics of the endangered hammerhead sharks Sphyrna mokarran and Sphyrna lewini of south Florida, USA. Chapt. 2, pp. 23–49, Universidad de los Andes, Santiago, Chile. Available at https://repositorio.uniandes.edu.co/server/api/core/bitstreams/4b57570c-23ae-4e8b-91b7-e422f53acd8e/content

Green ME, Appleyard SA, White W, Tracey S, Devloo-Delva F, Ovenden JR (2019) Novel multimarker comparisons address the genetic population structure of silvertip sharks (Carcharhinus albimarginatus). Marine and Freshwater Research 70, 1007-1019.
| Crossref | Google Scholar |

Green ME, Appleyard SA, White WT, Tracey SR, Heupel MR, Ovenden JR (2022) Updated connectivity assessment for the scalloped hammerhead (Sphyrna lewini) in Pacific and Indian Oceans using a multi-marker genetic approach. Fisheries Research 251, 106305.
| Crossref | Google Scholar |

Gruber B, Unmack PJ, Berry OF, Georges A (2018) dartR: an R package to facilitate analysis of SNP data generated from reduced representation genome sequencing. Molecular Ecology Resources 18, 691-699.
| Crossref | Google Scholar | PubMed |

Guttridge TL, Van Zinnicq Bergmann MPM, Bolte C, Howey LA, Finger JS, Kessel ST, Brooks JL, Winram W, Bond ME, Jordan LKB, Cashman RC, Tolentino ER, Grubbs RD, Gruber SH (2017) Philopatry and regional connectivity of the great hammerhead shark, Sphyrna mokarran in the US and Bahamas. Frontiers in Marine Science 4, 3.
| Crossref | Google Scholar |

Guttridge TL, Müller L, Keller BA, Bond ME, Grubbs RD, Winram W, Howey LA, Frazier BS, Gruber SH (2022) Vertical space use and thermal range of the great hammerhead (Sphyrna mokarran), (Rüppell, 1837) in the western north Atlantic. Journal of Fish Biology 101, 797-810.
| Crossref | Google Scholar | PubMed |

Harry AV, Tobin AJ, Simpfendorfer CA, Welch DJ, Mapleston A, White J, Williams AJ, Stapley J (2011) Evaluating catch and mitigating risk in a multispecies, tropical, inshore shark fishery within the Great Barrier Reef World Heritage Area. Marine and Freshwater Research 62, 710-721.
| Crossref | Google Scholar |

Heupel M, Simpfendorfer C, Chin A, Appleyard S, Barton D, Green M, Johnson G, McAuley R, White W (2020) Examination of connectivity of hammerhead sharks in northern Australia. Australian Institute of Marine Science, Townsville, Qld, Australia.

International Society of Genetic Genealogy (2020) Single-nucleotide polymorphism. (ISGG) Available at https://isogg.org/wiki/Single-nucleotide_polymorphism/en

Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403-1405.
| Crossref | Google Scholar | PubMed |

Kilian A, Wenzl P, Huttner E, Carling J, Xia L, Blois H, Caig V, Heller-Uszynska K, Jaccoud D, Hopper C, Aschenbrenner-Kilian M, Evers M, Peng K, Cayla C, Hok P, Uszynsk G (2012) Diversity arrays technology (DArT) – a generic genome profiling technology on open platforms. In ‘Data production and analysis in population genomics: methods and protocols’. (Eds F Pompanon, A Bonin) pp. 67–89. (Humana Press: New York, NY, USA)

Kraft DW, Conklin EE, Barba EW, Hutchinson M, Toonen RJ, Forsman ZH, Bowen BW (2020) Genomics versus mtDNA for resolving stock structure in the silky shark (Carcharhinus falciformis). PeerJ 8, e10186.
| Crossref | Google Scholar |

Luikart G, England PR, Tallmon D, Jordan S, Taberlet P (2003) The power and promise of population genomics: from genotyping to genome typing. Nature Reviews Genetics 4, 981-994.
| Crossref | Google Scholar | PubMed |

Maduna SN, Aspholm PE, Hansen A-SB, Klütsch CFC, Hagen SB (2024) Ecological niche modelling and population genomics provide insights into the geographic and demographic ‘explosion’ of a non-indigenous salmonid. Diversity and Distributions 30, e13811.
| Crossref | Google Scholar |

Marie AD, Stockwell BL, Rico C (2019) DNA analysis of Juvenile Scalloped Hammerhead Sharks Sphyrna lewini (Griffith, 1834) reveals multiple breeding populations and signs of adaptive divergence in the South Pacific. Frontiers in Marine Science 6, 718.
| Crossref | Google Scholar |

Miller M, Carlson J, Hogan L, Kobayashi D (2014) Status review report: great hammerhead shark (Sphyrna mokarran). (National Marine Fisheries Service and National Oceanic and Atmospheric Administration) Available at https://repository.library.noaa.gov/view/noaa/16286

National Oceanic and Atmospheric Administration (2022) Bathymetric data viewer. (NOAA, National Centers for Environmental Information) Available at https://www.ncei.noaa.gov/maps/bathymetry/ [Verified 30 October 2022]

Naylor GJP, Caira JN, Jensen K, Rosana KAM, White WT, Last PR (2012) A DNA sequence-based approach to the identification of shark and ray species and its implications for global elasmobranch diversity and parasitology. Bulletin of the American Museum of Natural History 367, 1-262.
| Crossref | Google Scholar |

Ovenden JR (2013) Crinkles in connectivity: combining genetics and other types of biological data to estimate movement and interbreeding between populations. Marine and Freshwater Research 64, 201-207.
| Crossref | Google Scholar |

Ovenden JR, 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.
| Crossref | Google Scholar | PubMed |

Pacoureau N, Rigby CL, Kyne PM, Sherley RB, Winker H, Carlson JK, Fordham SV, Barreto R, Fernando D, Francis MP, Jabado RW, Herman KB, Liu K-M, Marshall AD, Pollom RA, Romanov EV, Simpfendorfer CA, Yin JS, Kindsvater HK, Dulvy NK (2021) Half a century of global decline in oceanic sharks and rays. Nature 589, 567-571.
| Crossref | Google Scholar | PubMed |

Pembleton LW, Cogan NOI, Forster JW (2013) StAMPP: an R package for calculation of genetic differentiation and structure of mixed-ploidy level populations. Molecular Ecology Resources 13, 946-952.
| Crossref | Google Scholar | PubMed |

Queiroz N, Humphries NE, Mucientes G, Hammerschlag N, Lima FP, Scales KL, Miller PI, Sousa LL, Seabra R, Sims DW (2016) Ocean-wide tracking of pelagic sharks reveals extent of overlap with longline fishing hotspots. Proceedings of the National Academy of Sciences 113, 1582-1587.
| Crossref | Google Scholar |

Raoult V, Broadhurst MK, Peddemors VM, Williamson JE, Gaston TF (2019) Resource use of great hammerhead sharks (Sphyrna mokarran) off eastern Australia. Journal of Fish Biology 95, 1430-1440.
| Crossref | Google Scholar | PubMed |

Raoult V, Trueman CN, Kingsbury KM, Gillanders BM, Broadhurst MK, Williamson JE, Nagelkerken I, Booth DJ, Peddemors V, Couturier LIE, Gaston TF (2020) Predicting geographic ranges of marine animal populations using stable isotopes: a case study of great hammerhead sharks in eastern Australia. Frontiers in Marine Science 7, e594636.
| Crossref | Google Scholar |

Rigby C, Barreto R, Carlson J, Fernando D, Fordham S, Francis M, Herman K, Jabado R, Liu K, Marshall A, Pacoureau N, Romanov E, Sherley R, Winker H (2019) Great hammerhead Sphyrna mokarran. In ‘The IUCN Red List of Threatened Species 2019’. e.T39386A2920499. (International Union for Conservation of Nature and Natural Resources) Available at https://www.iucnredlist.org/es/species/39386/2920499

Roff G, Brown CJ, Priest MA, Mumby PJ (2018) Decline of coastal apex shark populations over the past half century. Communications Biology 1, 223.
| Crossref | Google Scholar |

Spaet JLY, Berumen ML (2015) Fish market surveys indicate unsustainable elasmobranch fisheries in the Saudi Arabian Red Sea. Fisheries Research 161, 356-364.
| Crossref | Google Scholar |

Stevens JD, Lyle JM (1989) Biology of three hammerhead sharks (Eusphyra blochii, Sphyrna mokarran and S. lewini) from Northern Australia. Marine and Freshwater Research 40, 129-146.
| Crossref | Google Scholar |

Testerman C (2014) Molecular ecology of globally distributed sharks. PhD thesis, Nova Southeastern University, Davie, FL, USA.

Testerman C, Prodöhl P, Shivji M (2008) Global phylogeography of the great (Sphyrna mokarran) and smooth (Sphyrna zygaena) hammerhead sharks. In ‘American Elasmobranch Society 24th Annual Meeting’, 27 July 2008, Montreal, QC, Canada. p. 130. (Nova Southeastern University: Fort Lauderdale, FL, USA)

Veríssimo A, Sampaio Í, McDowell JR, Alexandrino P, Mucientes G, Queiroz N, da Silva C, Jones CS, Noble LR (2017) World without borders—genetic population structure of a highly migratory marine predator, the blue shark (Prionace glauca). Ecology and Evolution 7, 4768-4781.
| Crossref | Google Scholar | PubMed |

Vince J, Hardesty BD, Wilcox C (2021) Progress and challenges in eliminating illegal fishing. Fish and Fisheries 22, 518-531.
| Crossref | Google Scholar |

Waples RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. Journal of Heredity 89, 438-450.
| Crossref | Google Scholar |

Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38, 1358-1370.
| Google Scholar | PubMed |