Pleistocene isolation, secondary introgression and restricted contemporary gene flow in the pig-eye shark, Carcharhinus amboinensis across northern Australia

Abstract

We examine the structure and phylogeography of the pig-eye shark (Carcharhinus amboinensis) common in shallow coastal environments in northern Australia using two types of genetic markers, two mitochondrial (control region and NADH hydrogenase 4) and two nuclear (microsatellite and Rag 1) DNA. Two populations were defined within northern Australia on the basis of mitochondrial DNA evidence, but this result was not supported by nuclear microsatellite or Rag 1 markers. One possibility for this structure might be sex-specific behaviours such as female philopatry, although we argue it is doubtful that sufficient time has elapsed for any potential signatures from this behaviour to be expressed in nuclear markers. It is more likely that the observed pattern represents ancient populations repeatedly isolated and connected during episodic sea level changes during the Pleistocene epoch, until current day with restricted contemporary gene flow maintaining population genetic structure. Our results show the need for an understanding of both the history and ecology of a species in order to interpret patterns in genetic structure.

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References

  1. Arevalo E, Davis SK, Sites JW (1994) Mitochondrial-DNA sequence divergence and phylogenetic-relationships among 8 chromosome races of the Sceloporus grammicus complex (Phrynosomatidae) in central Mexico. Syst Biol 43:387–418

    Google Scholar 

  2. Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography—the mitochondrial DNA bridge bewteen population-genetics and systematics. Annu Rev Ecol Syst 18:489–522

    Google Scholar 

  3. Carlson JK, Ribera MM, Conrath CL, Heupel MR, Burgess GH (2010) Habitat use and movement patterns of bull sharks, Carcharhinus leucas determined using po-up satellite archival tags. J Fish Biol 77:661–675

    PubMed  CAS  Google Scholar 

  4. Chapman DD, Babcock EA, Gruber SH, Dibattista JD, Franks BR, Kessel SA, Guttridge T, Pikitch EK, Feldheim KA (2009) Long-term natal site-fidelity by immature lemon sharks (Negaprion brevirostris) at a subtropical island. Mol Ecol 18:3500–3507

    PubMed  Article  Google Scholar 

  5. Chenoweth SF, Hughes JM, Keenan CP, Lavery S (1998) When oceans meet: a teleost shows secondary intergradation at an Indian-Pacific interface. Proceedings of the Royal Society of London Series B-Biological Sciences, vol 265, pp 415–420

  6. Clement M, Possada D, Crandall K (2000) TCS: a computer program to estimate genealogies. Mol Ecol 9:1657–1660

    Google Scholar 

  7. Cliff G, Dudley J (1991) Sharks caught in the protective nets off Natal, South Africa. 5. The Java Shark Carcharhinus amboinensis (Müller and Henle). S Afr J Mar Sci 11:443–453

    Article  Google Scholar 

  8. Cornuet JM, Luikart G (1997) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequence data. Genetics 144:2001–2014

    Google Scholar 

  9. Drummond AJ, Ashton B, Cheung M, Heled J, Kearse M, Moir R, Stones-Harves S, Thrierer T, Wilson A (2009) Geneious v4.65

  10. Duncan KM, Martin AP, Bowen BW, De Couet HG (2006) Global phylogeography of the scalloped hammerhead shark (Sphyrna lewini). Mol Ecol 15:2239–2251

    PubMed  Article  CAS  Google Scholar 

  11. Estoup A, Largiader CR, Perrot E, Chourrout D (1996) Rapid one-tube DNA extraction for reliable PCR detection of fish polymorphic markers and transgenes. Mol Mar Biol Biotechnol 5:295–298

    CAS  Google Scholar 

  12. Excoffier L, Laval G, Schneider S (2005) Arlequin ver 3.0. An integrated software package for population genetics data analysis. Evol Bioinformat Online 1:47–50

    CAS  Google Scholar 

  13. Feildheim KA, Gruber SH, Ashley MV (2002) The breeding biology of lemon shark at a tropical nursery lagoon. In: Proceedings of the royal society biolgical sciences, London, pp 1655–1661

  14. Feldheim KA, Gruber SH, Ashley MV (2004) Reconstruction of parental microsatellite genotypes reveals female polyandry and philopatry in the lemon shark, Negaprion brevirostris. Evolution 58:2332–2342

    PubMed  CAS  Google Scholar 

  15. Field IC, Meekan MG, Buckworth RC, Bradshaw CJA (2009) Protein mining the world’s oceans: Australasia as an example of illegal expansion-and-displacement fishing. Fish Fish 10:323–328

    Google Scholar 

  16. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to the conservation genetics. Cambridge University Press, Cambridge

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  18. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    PubMed  Article  CAS  Google Scholar 

  19. Inoue JG, Miya M, Tsukamoto K, Nishida M (2001) A mitogenomic perspective on the basal teleostean phylogeny: resolving higher-level relationships with longer DNA sequences. Mol Phylogenet Evol 20:275–285

    PubMed  Article  CAS  Google Scholar 

  20. IUCN (2010) Red list of threatened species. Version 2010.3

  21. Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:1–6

    Article  Google Scholar 

  22. 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

    PubMed  Article  CAS  Google Scholar 

  23. Kuhnt W, Holbourn A, Hall R, Zuvela M, Kase R (2004) Neogene history of the Indonesian throughflow. In: Clift P, Kuhnt W, Wang P, Hayes D (eds.) Continent–ocean interactions within East Asian Marginal Seas, pp 299–320

  24. Kumar S, Dudley J, Nei M, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Bioinformatics 9:299–306

    PubMed  CAS  Google Scholar 

  25. Last PR, Stevens JD (2009) Sharks and rays of Australia. CSIRO, Victoria

    Google Scholar 

  26. Lukoschek V, Waycott M, Marsh H (2007) Phylogeography of the olive sea snake, Aipysurus laevis (Hydrophiinae) indicates Pleistocene range expansion around northern Australia but low contemporary gene flow. Mol Ecol 16:3406–3422

    PubMed  Article  CAS  Google Scholar 

  27. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  28. Northern Territory Government (2009) Fishery status reports 2008. Department of Resources, Darwin

    Google Scholar 

  29. Ovenden JR, Street R, Broderick D (2006) New microsatellite loci for Carcharhinid sharks (Carcharhinus tilstoni and C-sorrah) and their cross-amplification in other shark species. Mol Ecol Notes 6:415–418

    Article  CAS  Google Scholar 

  30. Ovenden JR, Kashiwagi T, Broderick D, Giles J, Salini J (2009) The extent of population genetic subdivision differs among four co-distributed shark species in the Indo-Australian archipelago. BMC Evol Biol 9:40

    PubMed  Article  Google Scholar 

  31. Pardini AT, Jones CS, Noble LR, Kreiser B, Malcolm H, Bruce BD, Stevens JD, Cliff G, Scholl MC, Francis M, Duffy CAJ, Martin AP (2001) Sex-biased dispersal of great white sharks. Nature 412:139

    PubMed  Article  CAS  Google Scholar 

  32. Peakall R, Smouse PE (2005) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  33. 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. Mol Ecol 16:187–197

    PubMed  Article  CAS  Google Scholar 

  34. Possada D, Crandall KA (1998) Modeltest: testing the model of DNA substitutions. Bioinformatics 14:817–818

    Article  Google Scholar 

  35. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100

    PubMed  CAS  Google Scholar 

  36. Reynolds J, Weir BS, Cockerham CC (1983) Estimation of the co-ancestry coefficient—basis for a short-term genetic distance. Genetics 105:767–779

    PubMed  CAS  Google Scholar 

  37. Rozen S, Skaletsky H (2000) Primer 3 on the WWW for general users and for biologist programmers. Methods Mol Methodol 132:365–386

    CAS  Google Scholar 

  38. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234

    Google Scholar 

  39. 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 17:5336–5348

    PubMed  Article  CAS  Google Scholar 

  40. Slatkin M (1991) Inbreeding coefficients and coalescence times. Genet Res 58:167–175

    PubMed  Article  CAS  Google Scholar 

  41. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequences. Genetics 139:1463–1563

    Google Scholar 

  42. Swofford DL (2000) PAUP* phylogenetic analysis using parsimon (*and other methods). Sinauer Associates, Sunderland, MA

    Google Scholar 

  43. Tajima F (1983) Evolutionary relstionship of DNA sequences in finite populations. Genetics 123:585–595

    Google Scholar 

  44. Tajima F (1996) The amount of DNA polymorphism maintained in a finite population when the neutral mutation rate varies among sites. Genetics 143:1457–1465

    PubMed  CAS  Google Scholar 

  45. Tillett BJ, Parry DL, Munksgaard NC, Meekan MJ, Field IC, Bradshaw CJA, Thorburn D (2011) Decoding fingerprints—elemental composition of vertebrae map ontogenetic habitat partitioning between two morphologically similar apex predators in northern Australia. Mar Ecol Prog Ser 434:133–142

    Article  CAS  Google Scholar 

  46. Tillett BJ, Meekan MJ, Field I, Thorburn D, Ovenden J (in review) Evidence for reproductive philopatry in the bull shark, Carcharhinus leucas in northern Australia. J Fish Biol

  47. van Oosterhout C, Hutchinson WF, Wills PM, Siple P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  48. Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J Biogeogr 27:1153–1167

    Article  Google Scholar 

  49. Walsh PS, Metzger DA, Higuchi R (1991) Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513

    PubMed  CAS  Google Scholar 

  50. White WT, Last PR, Stevens JD, Yearsley GK, Fahmi, Dharmadi (2006) Economically important sharks and rays of Indonesia. CSIRO Publishing, Canberra

    Google Scholar 

  51. Williams M, Cook E, van der Kaars S, Barrows T, Shulmeister J, Kershaw P (2009) Glacial and deglacial climatic patterns in Australia and surrounding regions from 35000 to 10000 years ago reconstructed from terrestrial and near-shore proxy data. Quat Sci Rev 28:2398–2419

    Article  Google Scholar 

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Acknowledgments

Funded by Tropical Rivers and Coastal Knowledge Research Hub, Charles Darwin University, Darwin and the Molecular Fisheries Laboratory, Department of Employment, Economic Development and Innovation, Queensland Government. Sampling was undertaken with the kind support of fishermen; Wildlife Resources Inc; Kakadu National Park; Fishing and Fisheries Research, Centre James Cook University; Department of Fisheries—Western Australia, Fish for the Future, RSK Environment LTD/University of Bangor and the Department of Resources—Fisheries, Northern Territory. We also thank R. Street and J. Morgan for their technical expertise and Bioscience North Australia for their support.

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Tillett, B.J., Meekan, M.G., Broderick, D. et al. Pleistocene isolation, secondary introgression and restricted contemporary gene flow in the pig-eye shark, Carcharhinus amboinensis across northern Australia. Conserv Genet 13, 99–115 (2012). https://doi.org/10.1007/s10592-011-0268-z

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Keywords

  • Pleistocene
  • Secondary introgression
  • Predator
  • Carcharhinus spp.
  • Genetic structure
  • North Australia