Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE (Open Access)

Assessment of multiple paternity in spinner shark (Carcharhinus brevipinna) litters from eastern Australian waters

Alicia K. Linn https://orcid.org/0009-0009-0295-8531 A * , Alexis L. Levengood A , Christine L. Dudgeon B , Johan A. Gustafson A C , Julia L. Smith https://orcid.org/0000-0002-0723-0453 D and Bonnie J. Holmes A
+ Author Affiliations
- Author Affiliations

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

B University of the Sunshine Coast, School of Science, Technology and Engineering, Petrie, Moreton Bay, Qld 4502, Australia.

C Shark Ecology Australia, Robina, Gold Coast, Qld 4226, Australia.

D Griffith University, School of Environment and Science, Southport, Gold Coast, Qld 4215, Australia.

* Correspondence to: alicia.k.linn@gmail.com

Handling Editor: Colin Simpfendorfer

Marine and Freshwater Research 76, MF24222 https://doi.org/10.1071/MF24222
Submitted: 9 October 2024  Accepted: 1 July 2025  Published: 16 July 2025

© 2025 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

The spinner shark (Carcharhinus brevipinna) is a medium-sized, coastal species distributed across the warm waters of all ocean basins. Knowledge of this species’ reproductive biology is limited to general parameters such as reproductive mode and average litter sizes, and very little is known about their reproductive strategy.

Aims

Here, we provide an assessment of multiple paternity, using single nucleotide polymorphisms.

Methods

DNA was extracted from 2 gravid females and the 18 pups between their 2 litters captured off the Australian eastern coast. Sibship analyses were conducted to assess multiple paternity.

Key results

For the first time globally, multiple paternity was confirmed in this species in both litters examined.

Conclusions

This study confirms that C. brevipinna employs some degree of polyandry as part of its mating system.

Implications

This research contributes to the growing number of studies regarding multiple paternity in elasmobranchs and provides new information on the reproductive biology of this species.

Keywords: Carcharhinus brevipinna, elasmobranch, genetics, mating system, multiple sires, polyandry, reproductive biology, shark, single nucleotide polymorphisms, spinner shark.

References

Allen BR, Cliff G (2000) Sharks caught in the protective gill nets off Kwazulu–Natal, South Africa. 9. The spinner shark Carcharhinus brevipinna (Müller and Henle). South African Journal of Marine Science 22, 199-215.
| Crossref | Google Scholar |

Armada-Tapia S, Castillo-Geniz JL, Victoria-Cota N, Arce-Valdés LR, Enríquez-Paredes LM (2023) First evidence of multiple paternity in the blue shark (Prionace glauca). Journal of Fish Biology 102, 528-531.
| Crossref | Google Scholar | PubMed |

Byrne RJ, Avise JC (2012) Genetic mating system of the brown smoothhound shark (Mustelus henlei), including a literature review of multiple paternity in other elasmobranch species. Marine Biology 159, 749-756.
| Crossref | Google Scholar |

Capapé C, HEMIDA F, Seck AA, Diatta Y, Guélorget O, Zaouali J (2003) Distribution and reproductive biology of the spinner shark, Carcharhinus brevipinna (Müller & Henle, 1841) (Condrichthyes: Carcharhinidae). Israel Journal of Zoology 49, 269-286.
| Crossref | Google Scholar |

Coleman SW, Jones AG (2011) Patterns of multiple paternity and maternity in fishes. Biological Journal of the Linnean Society 103, 735-760.
| Crossref | Google Scholar |

Compagno LJV (1984) ‘FAO Fisheries Synopsis. Vol. 4. Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Part 2, Carcharhiniformes.’ (Food and Agriculture Organization of the United Nations: Rome, Italy)

Conrath C, Musick JA (2012) Reproductive biology of elasmobranchs. In ‘Biology of sharks and their relatives’, 2nd edn. (Eds JC Carrier, JA Musick, MR Heithaus) pp. 291–311. (CRC Press: Boca Raton, FL, USA)

Daly-Engel TS, Grubbs RD, Holland KN, Toonen RJ, Bowen BW (2006) Assessment of multiple paternity in single litters from three species of carcharhinid sharks in Hawaii. Environmental Biology of Fishes 76, 419-424.
| Crossref | Google Scholar |

Daly-Engel TS, Grubbs RD, Bowen BW, Toonen RJ (2007) Frequency of multiple paternity in an unexploited tropical population of sandbar sharks (Carcharhinus plumbeus). Canadian Journal of Fisheries and Aquatic Sciences 64, 198-204.
| Crossref | Google Scholar |

Daly-Engel TS, Grubbs RD, Feldheim KA, Bowen BW, Toonen RJ (2010) Is multiple mating beneficial or unavoidable? Low multiple paternity and genetic diversity in the shortspine spurdog Squalus mitsukurii. Marine Ecology Progress Series 403, 255-267.
| Crossref | Google Scholar |

Deeken D, Macdonald C, Gainsbury A, Green ML, Cassill DL (2024) Maternal risk-management elucidates the evolution of reproductive adaptations in sharks by means of natural selection. Scientific Reports 14, 20088.
| Crossref | Google Scholar |

Ebert DA, Dando M, Fowler S (2021) ‘Sharks of the world: a complete guide.’ (Princeton University Press)

Fitzpatrick JL, Kempster RM, Daly-Engel TS, Collin SP, Evans JP (2012) Assessing the potential for post-copulatory sexual selection in elasmobranchs. Journal of Fish Biology 80, 1141-1158.
| Crossref | Google Scholar | PubMed |

Frankham R (2005) Genetics and extinction. Biological Conservation 126, 131-140.
| Crossref | Google Scholar |

Geraghty PT, Williamson JE, Macbeth WG, Wintner SP, Harry AV, Ovenden JR, Gillings MR (2013) Population expansion and genetic structure in Carcharhinus brevipinna in the southern Indo-Pacific. PLoS ONE 8, e75169.
| Crossref | Google Scholar |

Geraghty PT, Macbeth WG, Williamson JE (2016) Aspects of the reproductive biology of dusky, spinner and sandbar sharks (family Carcharhinidae) from the Tasman Sea. Marine and Freshwater Research 67, 513-525.
| Crossref | Google Scholar |

Green ME, Appleyard SA, White W, Tracey S, Ovenden J (2017) Variability in multiple paternity rates for grey reef sharks (Carcharhinus amblyrhynchos) and scalloped hammerheads (Sphyrna lewini). Scientific Reports 7, 1528.
| 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 |

Hoekert WEJ, Neuféglise H, Schouten AD, Menken SBJ (2002) Multiple paternity and female-biased mutation at a microsatellite locus in the olive ridley sea turtle (Lepidochelys olivacea). Heredity 89, 107-113.
| Crossref | Google Scholar | PubMed |

Holmes BJ, Pope LC, Williams SM, Tibbetts IR, Bennett MB, Ovenden JR (2018) Lack of multiple paternity in the oceanodromous tiger shark (Galeocerdo cuvier). Royal Society Open Science 5, 171385.
| Crossref | Google Scholar |

Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biological Reviews of The Cambridge Philosophical Society 75, 21-64.
| Crossref | Google Scholar | PubMed |

Jones OR, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Molecular Ecology Resources 10, 551-555.
| Crossref | Google Scholar | PubMed |

Joung S, Liao Y, Liu K, Chen C, Leu L (2005) Age, growth, and reproduction of the spinner shark, Carcharhinus brevipinna, in the northeastern waters of Taiwan. Zoological Studies 44(1), 102-110 Available at https://zoolstud.sinica.edu.tw/Journals/44.1/102.html.
| Google Scholar |

Katona G, Szabó F, Végvári Z, Székely T, Jr, Liker A, Freckleton RP, Vági B, Székely T (2023) Evolution of reproductive modes in sharks and rays. Journal of Evolutionary Biology 36, 1630-1640.
| 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, Uszynski G (2012) Diversity arrays technology: a generic genome profiling technology on open platforms. In ‘Data production and analysis in population genomics: Methods and Protocols. Methods in Molecular Biology, Vol. 888’. (Eds F Pompanon, A Bonin) pp. 67–89. (Humana Press) doi:10.1007/978-1-61779-870-2_5

Klimley AP (2013) ‘The biology of sharks and rays.’ (The University of Chicago Press: London, UK)

Lamarca F, Carvalho PH, Vilasboa A, Netto-Ferreira AL, Vianna M (2020) Is multiple paternity in elasmobranchs a plesiomorphic characteristic? Environmental Biology of Fishes 103, 1463-1470.
| Crossref | Google Scholar |

Lamarca F, Carvalho PH, Netto-Ferreira AL (2024) The loss of female sperm storage ability as a potential driver for increased extinction in Chondrichthyes. Evolutionary Ecology 38, 461-479.
| Crossref | Google Scholar |

Legendre S (2004) Age structure, mating system, and population viability. In ‘Evolutionary conservation biology’. (Eds R Ferrière, U Dieckmann, D Couvet) pp. 41–58. (Cambridge University Press, International Institute for Applied Systems Analysis)

Lyons K, Chabot CL, Mull CG, Paterson Holder CN, Lowe CG (2017) Who’s my daddy? Considerations for the influence of sexual selection on multiple paternity in elasmobranch mating systems. Ecology and Evolution 7, 5603-5612.
| Crossref | Google Scholar | PubMed |

Lyons K, Kacev D, Mull CG (2021) An inconvenient tooth: evaluating female choice in multiple paternity using an evolutionarily and ecologically important vertebrate clade. Molecular Ecology 30, 1574-1593.
| Crossref | Google Scholar | PubMed |

Mull CG, Pennell MW, Yopak KE, Dulvy NK (2024) Maternal investment evolves with larger body size and higher diversification rate in sharks and rays. Current Biology 34, 2773-2781.E3.
| Crossref | Google Scholar | PubMed |

Nash CS, Darby PC, Frazier BS, Hendon JM, Higgs JM, Hoffmayer ER, Daly-Engel TS (2021) Multiple paternity in two populations of finetooth sharks (Carcharhinus isodon) with varying reproductive periodicity. Ecology and Evolution 11, 11799-11807.
| Crossref | Google Scholar | PubMed |

Neff BD, Pitcher TE (2005) Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Molecular Ecology 14, 19-38.
| Crossref | Google Scholar | PubMed |

Palmrose KK (2021) Reproductive biology of the spinner shark Carcharhinus brevipinna, off the Southeast US Coast. MSc thesis, University of North Florida, Jacksonville, FL, USA.

Pirog A, Magalon H, Poirout T, Jaquemet S (2019) Reproductive biology, multiple paternity and polyandry of the bull shark Carcharhinus leucas. Journal of Fish Biology 95, 1195-1206.
| Crossref | Google Scholar | PubMed |

Pirog A, Magalon H, Poirout T, Jaquemet S (2020) New insights into the reproductive biology of the tiger shark Galeocerdo cuvier and no detection of polyandry in Reunion Island, western Indian Ocean. Marine and Freshwater Research 71, 1301-1312.
| Crossref | Google Scholar |

Portnoy DS, Piercy AN, Musick JA, Burgess GH, Graves JE (2007) Genetic polyandry and sexual conflict in the sandbar shark, Carcharhinus plumbeus, in the western North Atlantic and Gulf of Mexico. Molecular Ecology 16, 187-197.
| Crossref | Google Scholar | PubMed |

Pratt HL, Jr, Carrier JC (2001) A review of elasmobranch reproductive behavior with a case study on the nurse shark, Ginglymostoma cirratum. Environmental Biology of Fishes 60, 157-188.
| Crossref | Google Scholar |

Premachandra HKA, Nguyen NH, Knibb W (2019) Effectiveness of SNPs for parentage and sibship assessment in polygamous yellowtail kingfish Seriola lalandi. Aquaculture 499, 24-31.
| Crossref | Google Scholar |

QIAGEN (2020) ‘DNeasy® blood & tissue handbook.’ (QIAGEN Inc.: Valencia, CA, USA)

Rigby CL, Carlson J, Smart JJ, Pacoureau N, Herman K, Derrick D, Brown E (2020) Spinner shark Carcharhinus brevipinna. In ‘The IUCN Red List of Threatened Species 2020’. e.T39368A2908817. (International Union for Conservation of Nature and Natural Resources) Available at https://www.iucnredlist.org/species/39368/2908817

Rossouw C, Wintner SP, Bester-Van Der Merwe AE (2016) Assessing multiple paternity in three commercially exploited shark species: Mustelus mustelus, Carcharhinus obscurus and Sphyrna lewini. Journal of Fish Biology 89, 1125-1141.
| Crossref | Google Scholar | PubMed |

Sansaloni C, Petroli C, Jaccoud D, Carling J, Detering F, Grattapaglia D, Kilian A (2011) Diversity Arrays Technology (DArT) and next-generation sequencing combined: genome-wide, high throughput, highly informative genotyping for molecular breeding of Eucalyptus. BMC Proceedings 5, P54.
| Crossref | Google Scholar |

Traylor-Holzer K (2021) Population viability analysis (PVA) report for population augmentation of Zebra Sharks (Stegostoma tigrinum) in Raja Ampat, Indonesia. IUCN SSC Conservation Planning Specialist Group, Apple Valley, MN, USA.

Wang J (2018) Estimating genotyping errors from genotype and reconstructed pedigree data. Methods in Ecology and Evolution 9, 109-120.
| Crossref | Google Scholar |

Wang J (2019) Pedigree reconstruction from poor quality genotype data. Heredity 122, 719-728.
| Crossref | Google Scholar | PubMed |

Williamson MJ, Dudgeon C, Slade R (2018) Tonic immobility in the zebra shark, Stegostoma fasciatum, and its use for capture methodology. Environmental Biology of Fishes 101, 741-748.
| Crossref | Google Scholar |