Deep mitochondrial lineage divergence among populations of the southern stingray (Hypanus americanus (Hildebrand & Schroeder, 1928)) throughout the Southeastern United States and Caribbean

Abstract

Although over half of all known elasmobranchs are batoids, with many species exploited and several of conservation concern, little is known of their population genetic structure and micro-evolutionary history. Here, we used sequence variation in 648 bp of the mitochondrial control region to study the phylogeography of the southern stingray (Hypanus americanus (Hildebrand & Schroeder, 1928)) (previously Dasyatis americana) throughout the Carolinas, Florida, and the Caribbean. Out of 267 individuals sampled from eight locations, 67 haplotypes were identified and analysis of molecular variance revealed a high level of genetic partitioning (ΦST = 0.49; P < 0.00001) that was delineated into three geographic regions: (i) the USA and Belize, (ii) the Bahamas and the West Indies, and (iii) Grand Cayman Islands. Phylogenetic and statistical parsimony analyses identified three divergent lineages that were largely concordant with the population structure. However, the geographic distribution of haplotypes described a complex phylogeographic pattern with numerous haplotypes from the divergent lineages co-occurring at the same sampling site. The strong genetic partitioning detected for the Grand Cayman population suggests that this small and isolated population might warrant individualized conservation management.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2

References

  1. Arlyza IS, Shen K-N, Durand J-D, Borsa P (2013) Mitochondrial haplotypes indicate parapatric-like phylogeographic structure in blue-spotted maskray (Neotrygon kuhlii) from the Coral Triangle region. J Hered 104:725–733

    Article  CAS  PubMed  Google Scholar 

  2. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge, MA, pp 3–37

  3. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57:289–300

    Google Scholar 

  4. Bensasson D, Zhang D-X, Hartl DL, Hewitt GM (2001) Mitochondrial pseudogenes: evolution’s misplaced witnesses. Trends Ecol Evol 16:314–321

    Article  CAS  PubMed  Google Scholar 

  5. Borsa P, Arlyza IS, Laporte M, Berrebi P (2012) Population genetic structure of blue-spotted maskray Neotrygon kuhlii and two other Indo-West Pacific stingray species (Myliobatiformes: Dasyatidae), inferred from size-polymorphic intron markers. J Exp Mar Biol Ecol 438:32–40

    Article  Google Scholar 

  6. Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Bowen BW, Shanker K, Yasuda N, Malay MCMD, von der Heyden S, Paulay G, Rocha LA, Selkoe KA, Barber PH, Williams ST (2014) Phylogeography unplugged: comparative surveys in the genomic era. Bull Mar Sci 90:13–46

    Article  Google Scholar 

  8. Castillo-Páez A, Sosa-Nishizaki O, Sandoval-Castillo J, Galván-Magaña F, Rocha-Olivares A (2014) Strong population structure and shallow mitochondrial phylogeny in the banded guitarfish, Zapteryx exasperata (Jordan y Gilbert, 1880), from the northern Mexican Pacific. J Hered 105:91–100

    Article  CAS  PubMed  Google Scholar 

  9. Chevolot M, Hoarau G, Rijnsdorp AD, Stam WT, Olsen JL (2006a) Phylogeography and population structure of thornback rays (Raja clavata L., Rajidae). Mol Ecol 15:3693–3705

    Article  CAS  PubMed  Google Scholar 

  10. Chevolot M, Ellis JR, Hoarau G, Rijnsdorp AD, Stam WT, Olsen JL (2006b) Population structure of the thornback ray (Raja clavata L.) in British waters. J Sea Res 56:305–316

    Article  Google Scholar 

  11. Chevolot M, Wolfs PH, Pálsson J, Rijnsdorp AD, Stam WT, Olsen JL (2007) Population structure and historical demography of the thorny skate (Amblyraja radiata, Rajidae) in the North Atlantic. Mar Biol 151:1275–1286

    Article  Google Scholar 

  12. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  CAS  PubMed  Google Scholar 

  13. Corcoran MJ, Wetherbee BM, Shivji MS, Potenski MD, Chapman DD, Harvey GM (2013) Supplemental feeding for ecotourism reverses diel activity and alters movement patterns and spatial distribution of the southern stingray, Dasyatis americana. PLoS One 8:e59235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. DeBiasse MB, Richards VP, Shivji MS, Hellberg ME (2016) Shared phylogeographical breaks in a Caribbean coral reef sponge and its invertebrate commensals. J Biogeogr 43:2136–2146

    Article  Google Scholar 

  15. Edwards SV (2009) Is a new and general theory of molecular systematics emerging? Evolution 63:1–19

    Article  CAS  PubMed  Google Scholar 

  16. Excoffier L, Lischer HE (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

    Article  Google Scholar 

  17. Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Griffiths AM, Sims DW, Cotterell SP, El Nagar A, Ellis JR, Lynghammar A, McHugh M, Neat FC, Pade NG, Queiroz N (2010) Molecular markers reveal spatially segregated cryptic species in a critically endangered fish, the common skate (Dipturus batis). Proc R Soc B Biol Sci 277:1497–1503

    Article  Google Scholar 

  19. Griffiths AM, Sims DW, Johnson A, Lynghammar A, McHugh M, Bakken T, Genner MJ (2011) Levels of connectivity between longnose skate (Dipturus oxyrinchus) in the Mediterranean Sea and the north-eastern Atlantic Ocean. Conserv Genet 12:577–582

    Article  Google Scholar 

  20. Hellberg M (2007) Footprints on water: the genetic wake of dispersal among reefs. Coral Reefs 26:463–473

    Article  Google Scholar 

  21. Hildebrand SF, Schroeder WC (1928) Fishes of Chesapeake Bay. Bulletin of the United States Bureau of Fisheries, 43(1):1–366

  22. Kashiwagi T, Marshall AD, Bennett MB, Ovenden JR (2012) The genetic signature of recent speciation in manta rays (Manta alfredi and M. birostris). Mol Phylogenet Evol 64:212–218

    Article  PubMed  Google Scholar 

  23. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  PubMed  PubMed Central  Google Scholar 

  24. 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

    Article  PubMed  Google Scholar 

  25. 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

    Article  PubMed  Google Scholar 

  26. 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 Biol Ecol 359:110–117

    Article  Google Scholar 

  27. Le Port A, Pawley M, Lavery S (2013) Speciation of two stingrays with antitropical distributions: low levels of divergence in mitochondrial DNA and morphological characters suggest recent evolution. Aquat Biol 19:153–165

    Article  Google Scholar 

  28. Li N, Song N, Cheng G-p, Gao T-x (2013) Genetic diversity and population structure of the red stingray, Dasyatis akajei inferred by AFLP marker. Biochem Syst Ecol 51:130–137

    Article  CAS  Google Scholar 

  29. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  30. Lynch-Stieglitz J, Curry WB, Slowey N (1999) Weaker Gulf Stream in the Florida straits during the last glacial maximum. Nature 402:644–648

    Article  CAS  Google Scholar 

  31. Mourier J, Planes S (2013) Direct genetic evidence for reproductive philopatry and associated fine-scale migrations in female blacktip reef sharks (Carcharhinus melanopterus) in French Polynesia. Mol Ecol 22:201–214

    Article  PubMed  Google Scholar 

  32. Neumann AC, Ball MM (1970) Submersible observations in the Straits of Florida: geology and bottom currents. Geol Soc Am Bull 81:2861–2874

    Article  Google Scholar 

  33. Newby J, Darden T, Shedlock AM (2014) Population genetic structure of spotted eagle rays, Aetobatus narinari, off Sarasota, Florida and the Southeastern United States. Copeia 2014:503–512

    Article  Google Scholar 

  34. Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:146–158

    Article  Google Scholar 

  35. Palva TK, Palva ET (1985) Rapid isolation of animal mitochondrial DNA by alkaline extraction. FEBS Lett 192:267–270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Phillips NM, Chaplin JA, Morgan DL, Peverell SC (2011) Population genetic structure and genetic diversity of three critically endangered Pristis sawfishes in Australian waters. Mar Biol 158:903–915

    Article  Google Scholar 

  37. Plank S, Lowe C, Feldheim K, Wilson R, Brusslan J (2010) Population genetic structure of the round stingray Urobatis halleri (Elasmobranchii: Rajiformes) in southern California and the Gulf of California. J Fish Biol 77:329–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Portnoy DS, McDowell JR, Heist EJ, Musick JA, Graves JE (2010) World phylogeography and male-mediated gene flow in the sandbar shark, Carcharhinus plumbeus. Mol Ecol 19:1994–2010

    Article  CAS  PubMed  Google Scholar 

  39. Puckridge M, Last PR, White WT, Andreakis N (2013) Phylogeography of the Indo-West Pacific maskrays (Dasyatidae, Neotrygon): a complex example of chondrichthyan radiation in the Cenozoic. Ecol Evol 3:217–232

    Article  PubMed  Google Scholar 

  40. Richards VP, Henning M, Witzell W, Shivji MS (2009) Species delineation and evolutionary history of the globally distributed spotted eagle ray (Aetobatus narinari). J Hered 100:273–283

    Article  CAS  PubMed  Google Scholar 

  41. Sandoval-Castillo J, Rocha-Olivares A (2011) Deep mitochondrial divergence in Baja California populations of an aquilopelagic elasmobranch: the golden cownose ray. J Hered 102:269–274

    Article  CAS  PubMed  Google Scholar 

  42. Sbisà E, Tanzariello F, Reyes A, Pesole G, Saccone C (1997) Mammalian mitochondrial D-loop region structural analysis: identification of new conserved sequences and their functional and evolutionary implications. Gene 205:125–140

    Article  PubMed  Google Scholar 

  43. Schluessel V, Broderick D, Collin S, Ovenden J (2010) Evidence for extensive population structure in the white-spotted eagle ray within the Indo-Pacific inferred from mitochondrial gene sequences. J Zool 281:46–55

    Article  Google Scholar 

  44. Sellas AB, Bassos-Hull K, Pérez-Jiménez JC, Angulo-Valdés JA, Bernal MA, Hueter RE (2015) Population structure and seasonal migration of the spotted eagle ray, Aetobatus narinari. J Hered 106:266–275

    Article  CAS  PubMed  Google Scholar 

  45. Smith W, Bizzarro J, Richards V, Nielsen J, Márquez-Flarías F, Shivji M (2009) Morphometric convergence and molecular divergence: the taxonomic status and evolutionary history of Gymnura crebripunctata and Gymnura marmorata in the eastern Pacific Ocean. J Fish Biol 75:761–783

    Article  CAS  PubMed  Google Scholar 

  46. Snelson FF Jr, Williams-Hooper SE, Schmid TH (1988) Reproduction and ecology of the Atlantic stingray, Dasyatis sabina, in Florida coastal lagoons. Copeia 1988:729–739

  47. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Stehmann M, McEachran J, Vergara R (1978) Dasyatidae. In: Fischer W (ed) FAO species identification sheets for fishery purposes Western Central Atlantic (Fishing Area 31). FAO, Rome

    Google Scholar 

  49. Struhsaker P (1969) Observations on the biology and distribution of the thorny stingray, Dasyatis centroura (Pisces: Dasyatidae). Bull Mar Sci 19:456–481

    Google Scholar 

  50. Templeton AR (2006) Population genetics and microevolutionary theory. John Wiley & Sons, Hoboken, NJ, pp 204–245

  51. Vaudo JJ, Wetherbee BM, Harvey GCM, Harvey JC, Prebble AJF, Corcoran MJ, Potenski MD, Bruni KA, Leaf RT, Henningsen AD, Collie JS, Shivji MS (2018) Characterisation and monitoring of one of the world’s most valuable ecotourism animals, the southern stingray at Stingray City, Grand Cayman. Mar Freshw Res 69:144–154

    Article  Google Scholar 

  52. Walker P, Howlett G, Millner R (1997) Distribution, movement and stock structure of three ray species in the North Sea and eastern English Channel. ICES J Mar Sci 54:797–808

    Article  Google Scholar 

Download references

Acknowledgements

We thank Dan Abel, Demian Chapman, Mark Corcoran, Brian DeAngelis, Jim Gelsleichter, Samuel Gruber, Alan Henningsen, Matt Potenski, Brad Wetherbee, and Tonya Wiley for collecting the samples and Steve Kish, Veronica Akle, Beth Babcock, Kevin Feldheim, Marcy Henning, Stephen Harrison, Scott Pikitch, Burr Heneman, and the staff of the WCS research facility at Glovers Reef, Belize, for the assistance in the field and laboratory. We thank Joseph Ryan for providing computation resources for portions of the analyses.

Funding

This research was supported by the Guy Harvey Ocean Foundation, NOAA Coastal Ocean Program, Nova Southeastern University National Coral Reef Institute, and the Pew Institute for Ocean Science.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Vincent P. Richards.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors.

Sampling and field studies

All necessary permits for sampling and observational field studies were obtained by the authors from the competent authorities and are mentioned in the acknowledgements, if applicable.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by R. Thiel

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Richards, V.P., DeBiasse, M.B. & Shivji, M. Deep mitochondrial lineage divergence among populations of the southern stingray (Hypanus americanus (Hildebrand & Schroeder, 1928)) throughout the Southeastern United States and Caribbean. Mar Biodiv 49, 1627–1634 (2019). https://doi.org/10.1007/s12526-018-0930-5

Download citation

Keywords

  • Batoid
  • Elasmobranch
  • Population structure
  • Conservation
  • Control region