Reviews in Fish Biology and Fisheries

, Volume 28, Issue 4, pp 941–951 | Cite as

Population genetics of the bigeye thresher shark Alopias superciliosus in the Atlantic and Indian Oceans: implications for conservation

  • Millke Jasmine Arminini Morales
  • Fernando Fernandes Mendonça
  • Carolina Oliveira Magalhães
  • Claudio Oliveira
  • Rui Coelho
  • Miguel Neves Santos
  • Vanessa Paes Cruz
  • Andrew Piercy
  • George Burgess
  • Fabio Vieira Hazin
  • Fausto Foresti
Research Paper


Population structure and genetic connectivity are pivotal contributions to the establishment of conservation strategies for fisheries management, in particular for highly migratory species that are affected by commercial fisheries. This study used partial sequences of mitochondrial DNA control region to determine the genetic structure of the bigeye thresher shark Alopias superciliosus in the Atlantic and Indian Oceans. A total of 858 base pairs of mtDNA CR from 228 individuals were analyzed. The resulting nucleotide diversity (π) was 0.0011 ± 0.0008 and the haplotype diversity (h) was 0.127 ± 0.030. These are the lowest diversities registered in elasmobranchs with this genetic marker. Two genetically distinct lineages were identified, one of them represented by 3.9% of the analyzed individuals and none restricted to any particular area. Simulated scenarios of population structure, tested with AMOVA and pairwise ΦST did not result in significant values indicating high connectivity among all sampled groups. The absence of population structure, even between Atlantic and Indian Oceans, corroborates the high dispersal ability of this species. The low genetic diversity detected in this species and the identification of two historical lineages occurring in sympatry, one represented by a very small number of individuals, should be considered in the conservation efforts and management plans of A. superciliosus.


Population genetics Conservation genetics Fisheries management Alopiidae Mitochondrial DNA 



The authors thank all those who contributed with this study, including anonymous reviewers. Sampling from the Portuguese fishery in the Atlantic and Indian Oceans was conducted by the Portuguese Institute for the Ocean and Atmosphere (IPMA), Portugal, within the scope of the European Data Collection Framework (PNAB/DCF). Thanks are also due to the technicians from IPMA for collecting and carefully handling samples during the Portuguese pelagic longline fishery observer program. R. Coelho is supported by an Investigador-FCT contract from the Portuguese Foundation for Science and Technology (FCT, Fundação para a Ciência e Tecnologia) supported by the EU European Social Fund and the Programa Operacional Potencial Humano (Ref: IF/00253/2014). This work was funded by FAPESP (Ref: BIOTA 2011/23787-0) and Project THRESHER (funded by FCT, Ref: PTDC/MAR/109915/2009).

Supplementary material

11160_2018_9531_MOESM1_ESM.docx (14 kb)
Table S1. Estimated values of pairwise ΦST among the eight locations of A. superciliosus (below the diagonal) and p values (above the diagonal). (DOCX 14 kb)


  1. Amorim A, Baum J, Cailliet GM, Clò S, Clarke SC, Fergusson I, Gonzalez M, Macias D, Mancini P, Mancusi C, Myers R, Reardon M, Trejo T, Vacchi M, Valenti SV (2009) Alopias superciliosus. In: IUCN 2011. IUCN red list of threatened species. Version 2011.2. Accessed 22 May 2016
  2. André C, Larsson LC, Laikre L, Bekkevold D, Brigham J, Carvalho GR, Dahlgren TG, Hutchinson WF, Mariani S, Mudde K, Ruzzante DE, Ryman N (2011) Detecting population structure in a high gene-flow species, Atlantic herring (Clupea harengus): direct, simultaneous evaluation of neutral vs putatively selected loci. Heredity 106(2):270–280CrossRefGoogle Scholar
  3. Andreotti S, Heyden S, Henriques R, Rutzen M, Meÿer M, Oosthuizen H, Matthee CA (2016) New insights into the evolutionary history of white sharks, Carcharodon carcharias. J Biogeogr 43(2):328–339CrossRefGoogle Scholar
  4. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16(1):37–48CrossRefGoogle Scholar
  5. Bernard AM, Feldheim KA, Heithaus MR, Wintner SP, Wetherbee BM, Shivji MS (2016) Global population genetic dynamics of a highly migratory, apex predator shark. Mol Ecol 25(21):5312–5329CrossRefGoogle Scholar
  6. Bernard AM, Horn RL, Chapman DD, Feldheim KA, Garla RC, Brooks EJ, Gore MA, Shivji MS (2017) Genetic connectivity of a coral reef ecosystem predator: the population genetic structure and evolutionary history of the Caribbean reef shark (Carcharhinus perezi). J Biogeogr 44(11):2488–2500CrossRefGoogle Scholar
  7. Brendtro KS, McDowell JR, Graves JE (2008) Population genetic structure of escolar (Lepidocybium flavobrunneum). Mar Biol 155(1):11–22CrossRefGoogle Scholar
  8. Camargo SM, Coelho R, Chapman D, Howey-Jordan L, Brooks EJ, Fernando D, Mendes NJ, Hazin FHV, Oliveira C, Santos MN, Foresti F, Mendonça FF (2016) Structure And genetic variability of the oceanic whitetip shark, Carcharhinus longimanus, determined using mitochondrial DNA. PLoS ONE 11(5):e0155623. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Camhi MD, Pikitch EK, Babcock EA (2008) Methods to improve understanding of pelagic sharks: demographics, assessment, and stock structure. In: Camhi MD, Pikitch EK, Babcock EA (eds) Sharks of the open ocean: biology, fisheries and conservation. Blackwell Publishing, Oxford, pp 285–287CrossRefGoogle Scholar
  10. Camhi MD, Valenti SV, Fordham SV, Fowler SL, Gibson C (2009) The conservation status of pelagic sharks and rays: report of the IUCN shark specialist group pelagic shark red list workshop. IUCN Species Survival Commission Shark Specialist Group, NewburyGoogle Scholar
  11. Cardeñosa D, Hyde J, Caballero S (2014) Genetic diversity and population structure of the pelagic thresher shark (Alopias pelagicus) in the Pacific Ocean: evidence for two evolutionarily significant units. PLoS ONE 9(10):e110193. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Chang CH, Shao KT, Lin YS, Ho HC, Liao YC (2014) The complete mitochondrial genome of the big-eye thresher shark, Alopias superciliosus (Chondrichthyes, Alopiidae). Mitochondrial DNA 25(4):290–292CrossRefGoogle Scholar
  13. Chen CT, Liu KM, Chang YC (1997) Reproductive biology of the bigeye thresher shark, Alopias superciliosus (Lowe, 1839) (Chondrichthyes: Alopiidae), in the northwestern Pacific. Ichthyol Res 44(2–3):227–235CrossRefGoogle Scholar
  14. Clarke CR, Karl SA, Horn RL, Bernard AM, Lea JS, Hazin FH, Prodöhl PA, Shivji MS (2015) Global mitochondrial DNA phylogeography and population structure of the silky shark, Carcharhinus falciformis. Mar Biol 162(5):945–955CrossRefGoogle Scholar
  15. Coelho R, Fernandez-Carvalho J, Lino PG, Santos MN (2012) An overview of the hooking mortality of elasmobranchs caught in a swordfish pelagic longline fishery in the Atlantic Ocean. Aquat Living Res 25(04):311–319CrossRefGoogle Scholar
  16. Compagno LJV (1984) FAO species catalogue, vol 4. Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Part 2—Carcharhiniformes. FAO Fish Synop 125(4/2):251–655. FAO, RomeGoogle Scholar
  17. Compagno LJV (2001) Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Bullhead, mackerel and carpet sharks (Heterodontiformes, Lamniformes and Orectolobiformes). In: FAO species catalogue for fishery purposes, vol 2. FAO, RomeGoogle Scholar
  18. Cortés E, Arocha F, Beerkircher L, Carvalho F, Domingo A, Heupel M, Holtzhausen H, Santos MN, Ribera M, Simpfendorfer C (2010) Ecological risk assessment of pelagic sharks caught in Atlantic pelagic longline fisheries. Aquat Living Res 23(1):25–34CrossRefGoogle Scholar
  19. Domingues RR, Hilsdorf AW, Shivji MM, Hazin FV, Gadig OB (2017) Effects of the Pleistocene on the mitochondrial population genetic structure and demographic history of the silky shark (Carcharhinus falciformis) in the western Atlantic Ocean. Rev Fish Biol Fish. CrossRefGoogle Scholar
  20. Dudgeon CL, Blower DC, Broderick D, Gile JL, Holmes BJ, Kashiwagi T, Krück NC, Morgan AT, Tillet BJ, Ovenden JR (2012) A review of the application of molecular genetics for fisheries management and conservation of sharks and rays. J Fish Biol 80(5):1789–1843CrossRefGoogle Scholar
  21. 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 Res 10(3):564–567CrossRefGoogle 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(2):479–491PubMedPubMedCentralGoogle Scholar
  23. Fernandez-Carvalho J, Coelho R, Mejuto J, Cortés E, Domingo A, Yokawa K, Liu K-M, García-Cortés B, Forselledo R, Ohshimo S, Ramos-Cartelle A, Tsai W-P, Santos NM (2015a) Pan-Atlantic distribution patterns and reproductive biology of the bigeye thresher, Alopias superciliosus. Rev Fish Biol Fish 25:551–568CrossRefGoogle Scholar
  24. Fernandez-Carvalho J, Coelho R, Erzini K, Santos MN (2015b) Modeling age and growth of the bigeye thresher (Alopias superciliosus) in the Atlantic Ocean. Fish B-NOAA 113:468–481Google Scholar
  25. Ferrette BLS, Mendonça FF, Coelho R, de Oliveira PGV, Hazin FHV, Romanov EV, Oliveira C, Santos MN, Foresti F (2015) High connectivity of the crocodile shark between the Atlantic and Southwest Indian Oceans: highlights for conservation. PLoS ONE 10(2):1–10Google Scholar
  26. Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147(2):915–925PubMedPubMedCentralGoogle Scholar
  27. Graves JE, McDowell JR (2006) Genetic analysis of white marlin (Tetrapturus albidus) stock structure. Bull Mar Sci 79(3):469–482Google Scholar
  28. Hoelzel AR, Shivji MS, Magnussen J, Francis MP (2006) Low worldwide genetic diversity in the basking shark (Cetorhinus maximus). Biol Lett 2(4):639–642CrossRefGoogle Scholar
  29. ICCAT (2013) Report of the inter-sessional meeting of the sharks species group. Mindelo, Cape Verde, 81 pp, 8–12 Apr 2013Google Scholar
  30. Ivanova NV, Dewaard JR, Hebert PD (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Mol Ecol Notes 6(4):998–1002CrossRefGoogle Scholar
  31. Karl SA, Castro ALF, Lopez JA, Charvet P, Burgess GH (2011) Phylogeography and conservation of the bull shark (Carcharhinus leucas) inferred from mitochondrial and microsatellite DNA. Conserv Genet 12(2):371–382CrossRefGoogle Scholar
  32. Karl SA, Castro AL, Garla RC (2012) Population genetics of the nurse shark (Ginglymostoma cirratum) in the western Atlantic. Mar Biol 159(3):489–498CrossRefGoogle Scholar
  33. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S et al (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649CrossRefGoogle Scholar
  34. Keeney DB, Heist EJ (2006) Worldwide phylogeography of the blacktip shark (Carcharhinus limbatus) inferred from mitochondrial DNA reveals isolation of western Atlantic populations coupled with recent Pacific dispersal. Mol Ecol 15(12):3669–3679CrossRefGoogle Scholar
  35. Li N, Chen X, Sun D, Song N, Lin Q, Gao T (2015) Phylogeography and population structure of the red stingray, Dasyatis akajei inferred by mitochondrial control region. Mitochondrial DNA 26(4):505–513CrossRefGoogle Scholar
  36. Liu KM, Chiang PJ, Chen CT (1998) Age and growth estimates of the bigeye thresher shark, Alopias superciliosus, in northeastern Taiwan waters. Fish B-NOAA 96(3):482–491Google Scholar
  37. Martínez P, González EG, Castilho R, Zardoya R (2006) Genetic diversity and historical demography of Atlantic bigeye tuna (Thunnus obesus). Mol Phylogenet Evol 39(2):404–416CrossRefGoogle Scholar
  38. Mcdowell JR, Carlsson JE, Graves JE (2007) Genetic analysis of blue marlin (Makaira nigricans) stock structure in the Atlantic Ocean. Gulf Caribb Res 19(2):75–82Google Scholar
  39. Mendonça FF, Oliveira C, Gadig OBF, Foresti F (2009) Populations analysis of the Brazilian Sharpnose Shark Rhizoprionodon lalandii (Chondrichthyes: Carcharhinidae) on the São Paulo coast, Southern Brazil: inferences from mt DNA sequences. Neotrop Ichthyol 7(2):213–216CrossRefGoogle Scholar
  40. Mendonça FF, Oliveira C, Gadig OB, Foresti F (2011) Phylogeography and genetic population structure of Caribbean sharpnose shark Rhizoprionodon porosus. Rev Fish Biol Fish 21(4):799–814CrossRefGoogle Scholar
  41. Nakano H, Matsunaga H, Okamoto H, Okazaki M (2003) Acoustic tracking of bigeye thresher shark Alopias superciliosus in the eastern Pacific Ocean. Mar Ecol Prog Ser 265:255–261CrossRefGoogle Scholar
  42. O’Leary SJ, Feldheim KA, Fields AT, Natanson LJ, Wintner S, Hussey N, Shivji MS, Chapman DD (2015) Genetic diversity of white sharks, Carcharodon carcharias, in the Northwest Atlantic and southern Africa. J Hered. CrossRefPubMedGoogle Scholar
  43. Pereyra S, García G, Miller P, Oviedo S, Domingo A (2010) Low genetic diversity and population structure of the narrownose shark (Mustelus schmitti). Fish Res 106(3):468–473CrossRefGoogle Scholar
  44. Petersen SL, Honig MB, Ryan PG, Underhill LG, Compagno LJ (2009) Pelagic shark bycatch in the tuna-and swordfish-directed longline fishery off southern Africa. Afr J Mar Sci 31(2):215–225CrossRefGoogle Scholar
  45. 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(4):903–915CrossRefGoogle Scholar
  46. 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(10):1994–2010CrossRefGoogle Scholar
  47. Portnoy DS, Hollenbeck CM, Belcher CN, Driggers WB, Frazier BS, Gelsleichter J, Grubbs RD, Gold JR (2014) Contemporary population structure and post-glacial genetic demography in a migratory marine species, the blacknose shark, Carcharhinus acronotus. Mol Ecol 23(22):5480–5495CrossRefGoogle Scholar
  48. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43(1):223–225CrossRefGoogle Scholar
  49. Schultz JK, Feldheim KA, Gruber SH, Ashley MV, McGovern TM, Bowen BW (2008) Global phylogeography and seascape genetics of the lemon sharks (genus Negaprion). Mol Ecol 17(24):5336–5348CrossRefGoogle Scholar
  50. Simpfendorfer C, Cortés E, Heupel M, Brooks E, Babcock E, Baum J, McAuley R, Dudley S, Stevens JD, Fordham S, Soldo A (2008) An integrated approach to determining the risk of overexploitation for data-poor pelagic Atlantic sharks. Expert Working Group Report, ICCATGoogle Scholar
  51. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3):585–595PubMedPubMedCentralGoogle Scholar
  52. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10(3):512–526PubMedGoogle Scholar
  53. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefGoogle Scholar
  54. Trejo T (2005) Global phylogeography of thresher sharks (Alopias spp.) inferred from mitochondrial DNA control region sequences. Doctoral dissertation, California State University Monterey BayGoogle Scholar
  55. Veríssimo A, Sampaio Í, McDowell JR, Alexandrino P, Mucientes G, Queiroz N, Silva C, Jones CS, Noble LR (2017) World without borders—genetic population structure of a highly migratory marine predator, the blue shark (Prionace glauca). Ecol Evol 7(13):4768–4781CrossRefGoogle Scholar
  56. Waples RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J Hered 89(5):438–450CrossRefGoogle Scholar
  57. Weng KC, Block BA (2004) Diel vertical migration of the bigeye thresher shark (Alopias superciliosus), a species possessing orbital retia mirabilia. Fish B-NOAA 102(1):221–229Google Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Millke Jasmine Arminini Morales
    • 1
  • Fernando Fernandes Mendonça
    • 2
  • Carolina Oliveira Magalhães
    • 1
  • Claudio Oliveira
    • 1
  • Rui Coelho
    • 3
    • 4
  • Miguel Neves Santos
    • 3
  • Vanessa Paes Cruz
    • 1
  • Andrew Piercy
    • 5
  • George Burgess
    • 6
  • Fabio Vieira Hazin
    • 7
  • Fausto Foresti
    • 1
  1. 1.Laboratório de Biologia e Genética de Peixes, Instituto de Biociências de BotucatuUniversidade Estadual Paulista (UNESP)BotucatuBrazil
  2. 2.Laboratório de Genética Pesqueira e Conservação, Instituto do MarUniversidade Federal de São Paulo (UNIFESP)SantosBrazil
  3. 3.Instituto Português do Mar e da Atmosfera (IPMA)OlhãoPortugal
  4. 4.Centro de Ciências do Mar (CCMAR)Universidade do AlgarveFaroPortugal
  5. 5.Lake Nona CampusValencia CollegeOrlandoUSA
  6. 6.Florida Museum of Natural History, Florida Program for Shark ResearchUniversity of FloridaGainesvilleUSA
  7. 7.Departamento de Pesca e AquiculturaUniversidade Federal Rural de Pernambuco (UFRPE)RecifeBrazil

Personalised recommendations