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.
Buy single article
Instant access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
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
Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge, MA, pp 3–37
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
Bensasson D, Zhang D-X, Hartl DL, Hewitt GM (2001) Mitochondrial pseudogenes: evolution’s misplaced witnesses. Trends Ecol Evol 16:314–321
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
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
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
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
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
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
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
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659
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
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
Edwards SV (2009) Is a new and general theory of molecular systematics emerging? Evolution 63:1–19
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
Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
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
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
Hellberg M (2007) Footprints on water: the genetic wake of dispersal among reefs. Coral Reefs 26:463–473
Hildebrand SF, Schroeder WC (1928) Fishes of Chesapeake Bay. Bulletin of the United States Bureau of Fisheries, 43(1):1–366
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
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
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
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
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
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
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
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Lynch-Stieglitz J, Curry WB, Slowey N (1999) Weaker Gulf Stream in the Florida straits during the last glacial maximum. Nature 402:644–648
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
Neumann AC, Ball MM (1970) Submersible observations in the Straits of Florida: geology and bottom currents. Geol Soc Am Bull 81:2861–2874
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
Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:146–158
Palva TK, Palva ET (1985) Rapid isolation of animal mitochondrial DNA by alkaline extraction. FEBS Lett 192:267–270
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
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
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
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
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
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
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
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
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
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
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
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313
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
Struhsaker P (1969) Observations on the biology and distribution of the thorny stingray, Dasyatis centroura (Pisces: Dasyatidae). Bull Mar Sci 19:456–481
Templeton AR (2006) Population genetics and microevolutionary theory. John Wiley & Sons, Hoboken, NJ, pp 204–245
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
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
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.
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.
Conflict of interest
The authors declare that they have no conflict of interest.
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.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Communicated by R. Thiel
About this article
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
- Population structure
- Control region