Conservation Genetics

, Volume 20, Issue 4, pp 717–728 | Cite as

Population structure and male-biased dispersal in the short-tail stingray Bathytoshia brevicaudata (Myliobatoidei: Dasyatidae)

  • Emily J. RoycroftEmail author
  • Agnès Le Port
  • Shane D. Lavery
Research Article


Selective pressures driving dispersal in vagile species often differ between males and females, resulting in sex-biased dispersal. Male-biased dispersal is common in mammals, where there is greater reproductive investment by females, and there is emerging evidence for a similar pattern in elasmobranchs. We examine the population structure of the short-tail stingray (Bathytoshia brevicaudata), a large, viviparous coastal species common in southern hemisphere waters. Using 11 nuclear (nDNA) microsatellite markers from 202 individuals in comparison to mitochondrial (mtDNA) data reported by Le Port and Lavery (J Hered 103:174–185, 2012), we elucidate patterns of dispersal at both southern hemisphere and New Zealand scales. At a global scale, estimates of population differentiation were comparable across marker types (microsatellite FST = 0.148, p < 0.001, mtDNA ϕST = 0.67, p < 0.001). In contrast, New Zealand structure was much weaker for microsatellite markers (FST = 0.0026, p > 0.05) than for mtDNA (ϕST = 0.054, p < 0.05). Female-only data displayed a greater degree of population differentiation from both nDNA and mtDNA compared to male-only data, and population assignment tests indicated that males were significantly more likely to be immigrants to the population from which they were sampled. We estimate that within New Zealand, male-mediated gene flow is at least fivefold greater than female-mediated gene flow. This molecular evidence for sex-biased dispersal in a batoid species adds further support to male-biased dispersal as a recurrent pattern in viviparous elasmobranchs. Many elasmobranch species are vulnerable to extinction, and understanding movement patterns is crucial to management of threatened populations.


Dasyatis brevicaudata Smooth stingray Coastal stingray Microsatellite Population genetics Sex-biased dispersal 



Many thanks to the skippers of R/V Hawere, B. Doak and M. Birch, and to N. Hannam, S. Tindale and J. Dick for their invaluable help in New Zealand field collections. Thanks to M. Smale, L. Singh, C. Duffy, P. Last, W. White, A. Graham, D. Phillips and D. Chapman for the contribution of overseas samples. We are grateful to V. Thakur, B. Yellapu and V. Arranz Martínez for their generous advice and assistance with laboratory protocols and analysis, and to three anonymous reviewers who provided considered comments that greatly improved the final version of our manuscript.

Compliance with ethical standards

Ethical approval

All procedures were conducted under the animal care protocols approved by the University of Auckland Animal Ethics Committee (AEC Permits R240 & R1067), and research within the Poor Knights Islands Marine Reserve was conducted under Department of Conservation Permit no. NO-14234-RES.

Supplementary material

10592_2019_1167_MOESM1_ESM.xlsx (27 kb)
Supplementary material 1 (XLSX 26 KB)
10592_2019_1167_MOESM2_ESM.pdf (141 kb)
Supplementary material 2 (PDF 141 KB)
10592_2019_1167_MOESM3_ESM.pdf (147 kb)
Supplementary material 3 (PDF 146 KB)
10592_2019_1167_MOESM4_ESM.pdf (112 kb)
Supplementary material 4 (PDF 112 KB)
10592_2019_1167_MOESM5_ESM.pdf (900 kb)
Supplementary material 5 (PDF 900 KB)


  1. Ahonen H, Harcourt RG, Stow AJ (2009) Nuclear and mitochondrial DNA reveals isolation of imperilled grey nurse shark populations (Carcharias taurus). Mol Ecol 18:4409–4421. CrossRefPubMedGoogle Scholar
  2. Andreotti S, Von Der Heyden S, Henriques R et al (2016) New insights into the evolutionary history of white sharks, Carcharodon carcharias. J Biogeogr 43:328–339. CrossRefGoogle Scholar
  3. Arlt D, Pärt T (2008) Sex-biased dispersal: a result of a sex difference in breeding site availability. Am Nat 171:844–850. CrossRefPubMedGoogle Scholar
  4. Banks SC, Peakall R (2012) Genetic spatial autocorrelation can readily detect sex-biased dispersal. Mol Ecol 21:2092–2105. CrossRefPubMedGoogle Scholar
  5. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300Google Scholar
  6. Bester-van der Merwe AE, Bitalo D, Cuevas JM et al (2017) Population genetics of Southern Hemisphere tope shark (Galeorhinus galeus): intercontinental divergence and constrained gene flow at different geographical scales. PLoS ONE 12:1–20. CrossRefGoogle Scholar
  7. Birky CW (2001) The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms and models. Annu Rev Genet 35:125–148CrossRefPubMedGoogle Scholar
  8. Blower DC, Pandolfi JM, Bruce BD et al (2012) Population genetics of Australian white sharks reveals fine-scale spatial structure, transoceanic dispersal events and low effective population sizes. Mar Ecol Ser 455:229–244. CrossRefGoogle Scholar
  9. Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74:21–45CrossRefPubMedGoogle Scholar
  10. Bradbury IR, Laurel B, Snelgrove PV et al (2008) Global patterns in marine dispersal estimates: the influence of geography, taxonomic category and life history. Proc R Soc B Biol Sci 275:1803–1809. CrossRefGoogle Scholar
  11. Bräutigam A, Callow M, Campbell IR et al (2015) Global Priorities for Conserving Sharks and Rays: A 2015–2025 Strategy. k0agd_GSRI_GlobalPrioritiesForConservingSharksAndRays_web_singles.pdf
  12. Cabral RB, Gaines SD, Lim MT et al (2016) Siting marine protected areas based on habitat quality and extent provides the greatest benefit to spatially structured metapopulations. Ecosphere. CrossRefGoogle Scholar
  13. 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. Ann Rev Mar Sci 7:547–570. CrossRefPubMedGoogle Scholar
  14. Clarke AL, Sæther B-E, Røskaft E (1997) Sex biases in avian dispersal: a reappraisal. Oikos 79:429–438. CrossRefGoogle Scholar
  15. Clutton-Brock TH, Lukas D (2012) The evolution of social philopatry and dispersal in female mammals. Mol Ecol 21:472–492. CrossRefGoogle Scholar
  16. Daly-Engel TS, Seraphin KD, Holland KN et al (2012) Global phylogeography with mixed-marker analysis reveals male-mediated dispersal in the endangered scalloped hammerhead shark (Sphyrna lewini). PLoS One 7:279–289. CrossRefGoogle Scholar
  17. Dobson FS (2013) The enduring question of sex-biased dispersal: Paul J. Greenwood’s (1980) seminal contribution. Anim Behav 85:299–304. CrossRefGoogle Scholar
  18. Dulvy NK, Fowler SL, Musick JA et al (2014) Extinction risk and conservation of the world’s sharks and rays. Elife 3:e00590. CrossRefPubMedPubMedCentralGoogle Scholar
  19. Dulvy NK, Simpfendorfer CA, Davidson LNK et al (2017) Challenges and priorities in shark and ray conservation. Curr Biol 27:R565–R572. CrossRefPubMedGoogle Scholar
  20. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. CrossRefGoogle Scholar
  21. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. CrossRefGoogle Scholar
  22. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Farhadi A, Jeffs AG, Farahmand H et al (2017) Mechanisms of peripheral phylogeographic divergence in the indo-Pacific: lessons from the spiny lobster Panulirus homarus. BMC Evol Biol 17:195. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Favre L, Balloux F, Goudet J, Perrin N (1997) Female-biased dispersal in the monogamous mammal Crocidura russula: evidence from field data and microsatellite patterns. Proc R Soc B Biol Sci 264:127–132. CrossRefGoogle Scholar
  25. Flowers K, Ajemian M, Bassos-Hull K et al (2016) A review of batoid philopatry, with implications for future research and population management. Mar Ecol Prog Ser 562:251–261. CrossRefGoogle Scholar
  26. Goudet J, Perrin N, Waser P (2002) Tests for sex-biased dispersal using bi-parentally inherited genetic markers. Mol Ecol 11:1103–1114. CrossRefPubMedGoogle Scholar
  27. Gowaty PA (1993) Differential dispersal, local resource competition, and sex ratio variation in birds. Am Nat 141:263–280. CrossRefGoogle Scholar
  28. Grant SW, Bowen BW (2006) Living in a tilted world: climate change and geography limit speciation in Old World anchovies (Engraulis; Engraulidae). Biol J Linn Soc 88:673–689. CrossRefGoogle Scholar
  29. Green ME, D’Anastasi BR, Hobbs JPA et al (2018) Mixed-marker approach suggests maternal philopatry and sex-biased behaviours of narrow sawfish Anoxypristis cuspidata. Endanger Species Res 37:45–54. CrossRefGoogle Scholar
  30. Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162. CrossRefGoogle Scholar
  31. Grewe PM, Smolenski AJ, Ward RD (1994) Mitochondrial DNA diversity in Jackass Morwong (Nemadactylus macropterus: Teleostei) from Australian and New Zealand waters. Can J Fish Aquat Sci 51:1101–1109. CrossRefGoogle Scholar
  32. Hedrick PW, Allendorf FW, Baker CS (2013) Estimation of male gene flow from measures of nuclear and female genetic differentiation. J Hered 104:713–717. CrossRefPubMedGoogle Scholar
  33. Hernández S, Daley R, Walker T et al (2015) Demographic history and the South Pacific dispersal barrier for school shark (Galeorhinus galeus) inferred by mitochondrial DNA and microsatellite DNA mark. Fish Res 167:132–142. CrossRefGoogle Scholar
  34. Heupel MR, Carlson JK, Simpfendorfer CA (2007) Shark nursery areas: concepts, definition, characterization and assumptions. Mar Ecol Prog Ser 337:287–297. CrossRefGoogle Scholar
  35. Hueter RE, Heupel MR, Heist EJ, Keeney DB (2005) Evidence of philopatry in sharks and implications for the management of shark fisheries. J Northwest Atl Fish Sci 35:239–247. CrossRefGoogle Scholar
  36. Iglésias SP, Toulhoat L, Sellos DY (2010) Taxonomic confusion and market mislabelling of threatened skates: important consequences for their conservation status. Aquat Conserv Mar Freshw Ecosyst 20:319–333. CrossRefGoogle Scholar
  37. Jacoby DMP, Croft DP, Sims DW (2012) Social behaviour in sharks and rays: analysis, patterns and implications for conservation. Fish Fish 13:399–417. CrossRefGoogle Scholar
  38. Jorgensen SJ, Reeb CA, Chapple TK et al (2010) Philopatry and migration of Pacific white sharks. Proc R Soc B Biol Sci 277:679–688. CrossRefGoogle Scholar
  39. Kearse M, Moir R, Wilson A et al (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Keeney DB, Heupel MR, Hueter RE, Heist EJ (2005) Microsatellite and mitochondrial DNA analyses of the genetic structure of blacktip shark (Carcharhinus limbatus) nurseries in the northwestern Atlantic, Gulf of Mexico, and Caribbean Sea. Mol Ecol 14:1911–1923. CrossRefPubMedGoogle Scholar
  41. Kopelman NM, Mayzel J, Jakobsson M et al (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191. CrossRefPubMedPubMedCentralGoogle Scholar
  42. Larsson LC, Charlier J, Laikre L, Ryman N (2009) Statistical power for detecting genetic divergence-organelle versus nuclear markers. Conserv Genet 10:1255–1264. CrossRefGoogle Scholar
  43. Last PR, Stevens JD (2009) Sharks and rays of Australia, 2nd edn. CSIRO Publishing, CollingwoodGoogle Scholar
  44. Last PR, Naylor GJP, Manjaji-Matsumoto BM (2016) A revised classification of the family Dasyatidae (Chondrichthyes: Myliobatiformes) based on new morphological and molecular insights. Zootaxa 4139:345–368. CrossRefPubMedGoogle Scholar
  45. Lawson Handley LJ, Perrin N (2007) Advances in our understanding of mammalian sex-biased dispersal. Mol Ecol 16:1559–1578. CrossRefGoogle Scholar
  46. Le Port A, Lavery S (2012) Population structure and phylogeography of the short-tailed stingray, Dasyatis brevicaudata (Hutton 1875), in the Southern Hemisphere. J Hered 103:174–185. CrossRefPubMedGoogle Scholar
  47. Le Port A, Sippel T, Montgomery JC (2008) Observations of mesoscale movements in the short-tailed stingray, Dasyatis brevicaudata from New Zealand using a novel PSAT tag attachment method. J Exp Mar Bio Ecol 359:110–117CrossRefGoogle Scholar
  48. Le Port A, Lavery S, Montgomery JC (2012) Conservation of coastal stingrays: seasonal abundance and population structure of the short-tailed stingray Dasyatis brevicaudata at a Marine Protected Area. ICES J Mar Sci 69:1427–1435CrossRefGoogle Scholar
  49. Le Port A, Roycroft EJ, Thakur V, Lavery SD (2016) Characterisation of eleven new polymorphic microsatellite markers for the coastal stingray Dasyatis brevicaudata (Dasyatidae Hutton 1875), and cross-amplification in seven dasyatid species. Biochem Syst Ecol 65:234–237. CrossRefGoogle Scholar
  50. Mabry KE, Shelley EL, Davis KE et al (2013) Social mating system and sex-biased dispersal in mammals and birds: a phylogenetic analysis. PLoS One 8:e57980. CrossRefPubMedPubMedCentralGoogle Scholar
  51. Macbeth GM, Broderick D, Ovenden JR, Buckworth RC (2011) Likelihood-based genetic mark-recapture estimates when genotype samples are incomplete and contain typing errors. Theor Popul Biol 80:185–196. CrossRefPubMedGoogle Scholar
  52. Moritz C (1994) Defining ‘evolutionarily significant units’ for conservation. Trends Ecol Evol 9:373–375CrossRefPubMedGoogle Scholar
  53. Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354. CrossRefGoogle Scholar
  54. Pardini AT, Jones CS, Noble LR et al (2001) Sex-biased dispersal of great white sharks. Nature 412:139–140. CrossRefPubMedGoogle Scholar
  55. Payevsky VA (2016) Sex-biased survival and philopatry in birds: Do they interact? Biol Bull 43:804–818. CrossRefGoogle Scholar
  56. Peakall R, Smouse PE (2006) GENALEX 6: Genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. CrossRefGoogle Scholar
  57. Peakall R, Smouse PE (2012) GenALEx 6.5: Genetic analysis in excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539. CrossRefPubMedPubMedCentralGoogle Scholar
  58. Perrin N, Mazalov V (2000) Local competition, inbreeding, and the evolution of sex-biased dispersal. Am Nat 155:116–127CrossRefGoogle Scholar
  59. Phillips NM, Chaplin JA, Peverell SC, Morgan DL (2017) Contrasting population structures of three Pristis sawfishes with different patterns of habitat use. Mar Freshw Res 68:452–460. CrossRefGoogle Scholar
  60. Planes S, Jones GP, Thorrold SR (2009) Larval dispersal connects fish populations in a network of marine protected areas. Proc Natl Acad Sci 106:5693–5697. CrossRefPubMedGoogle Scholar
  61. Portnoy DS, Heist EJ (2012) Molecular markers: progress and prospects for understanding reproductive ecology in elasmobranchs. J Fish Biol 80:1120–1140. CrossRefPubMedGoogle Scholar
  62. Portnoy DS, Puritz JB, Hollenbeck CM et al (2015) Selection and sex-biased dispersal: the influence of philopatry on adaptive variation. PeerJ. CrossRefGoogle Scholar
  63. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959. CrossRefPubMedPubMedCentralGoogle Scholar
  64. Prugnolle F, DeMeeus T (2002) Inferring sex-biased dispersal from population genetic tools: a review. Heredity 88:161–165. CrossRefGoogle Scholar
  65. Pusey AE (1987) Sex-biased dispersal and inbreeding avoidance in birds and mammals. Trends Ecol Evol 2:295–299. CrossRefPubMedGoogle Scholar
  66. Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106. CrossRefPubMedPubMedCentralGoogle Scholar
  67. Ryman N, Palm S (2006) POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Mol Ecol 6:600–602. CrossRefGoogle Scholar
  68. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a labortatory manual. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  69. Schrey AW, Heist EJ (2003) Microsatellite analysis of population structure in the shortfin mako (Isurus oxyrinchus). Can J Fish Aquat Sci 60:670–675. CrossRefGoogle Scholar
  70. Sellas AB, Bassos-hull K, Pérez-jiménez JC et al (2015) Population structure and seasonal migration of the spotted eagle ray, Aetobatus narinari. J Hered. CrossRefPubMedGoogle Scholar
  71. Simpfendorfer CA, Milward NE (1993) Utilisation of a tropical bay as a nursery area by sharks of the families Carcharhinidae and Sphyrnidae. Environ Biol Fishes 37:337–345. CrossRefGoogle Scholar
  72. Slatkin M (1985) Gene flow in natural populations. Annu Rev Ecol Syst 16:393–430CrossRefGoogle Scholar
  73. Tillett J, Meekan MG, Field IC et al (2012) Evidence for reproductive philopatry in the bull shark Carcharhinus leucas. J Fish Biol 80:2140–2158. CrossRefPubMedGoogle Scholar
  74. Toews DPL, Brelsford A (2012) The biogeography of mitochondrial and nuclear discordance in animals. Mol Ecol 21:3907–3930. CrossRefPubMedGoogle Scholar
  75. Trochet A, Stevens VM, Baguette M (2016) Evolution of sex-biased dispersal. Q Rev Biol 91:297–320CrossRefPubMedGoogle Scholar
  76. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: Software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538. CrossRefGoogle Scholar
  77. Veríssimo A, McDowell JR, Graves JE (2012) Genetic population structure and connectivity in a commercially exploited and wide-ranging deepwater shark, the leafscale gulper (Centrophorus squamosus). Mar Freshw Res 63:505. CrossRefGoogle Scholar
  78. von der Heyden S, Lipinski MR, Matthee CA (2010) Remarkably low mtDNA control region diversity in an abundant demersal fish. Mol Phylogenet Evol 55:1183–1188. CrossRefPubMedGoogle Scholar
  79. Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia: Shorelines, river systems and time durations. J Biogeogr 27:1153–1167. CrossRefGoogle Scholar
  80. Ward RD, Elliott NG (2001) Genetic population structure of species in the South East Fishery of Australia. Mar Freshw Res 52:563–573. CrossRefGoogle Scholar
  81. Waters JM, McCulloch GA, Eason JA (2007) Marine biogeographical structure in two highly dispersive gastropods: implications for trans-Tasman dispersal. J Biogeogr 34:678–687. CrossRefGoogle Scholar
  82. Weir BS, Cockerham C (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370Google Scholar
  83. Wourms JI, Demski LS (1993) The reproduction and development of sharks, skates, rays and ratfishes: introduction, history, overview, and future prospects. Environ Biol Fishes 38:7–21CrossRefGoogle Scholar
  84. Zink RM, Barrowclough GF (2008) Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 17:2107–2121. CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.School of Biological SciencesUniversity of AucklandAucklandNew Zealand
  2. 2.Sciences DepartmentMuseums VictoriaMelbourneAustralia
  3. 3.School of BioSciencesUniversity of MelbourneParkvilleAustralia
  4. 4.Institute of Marine Science, Leigh Marine LaboratoryUniversity of AucklandWarkworthNew Zealand
  5. 5.Centre for Sustainable Tropical Fisheries and AquacultureJames Cook UniversityTownsvilleAustralia

Personalised recommendations