Skip to main content
SpringerLink
Log in

Population genetic structure and genetic diversity of three critically endangered Pristis sawfishes in Australian waters

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Northern Australia is considered to be one of the last strongholds for three critically endangered sawfishes, Pristis zijsron, Pristis clavata, and Pristis microdon, making these populations of global significance. Population structure and levels of genetic diversity were assessed for each species across northern Australia using a portion of the mitochondrial control region. Statistically significant genetic structure was detected in all three species, although it was higher in P. microdon (F ST = 0.811; N = 149) than in either P. clavata (F ST = 0.419; N = 73) or P. zijsron (F ST = 0.202; N = 49), possibly due to a much higher and/or localized level of female philopatry in P. microdon. The overall levels of haplotype diversity in P. zijsron (h = 0.555), P. clavata (h = 0.489), and P. microdon (h = 0.650) were moderate, although it appears to be reduced in the assemblages of P. zijsron and P. clavata in the Gulf of Carpentaria (h = 0.342 and h = 0.083, respectively). Since female migration (replenishment) between regions is unlikely, conservation plans should strive to maintain current levels of diversity and abundances in the regional assemblages of each species.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Amos W, Balmford A (2001) When does conservation genetics matter? Heredity 87:257–265

    Article  CAS  Google Scholar 

  • Bruce BD, Stevens JD, Malcolm H (2006) Movements and swimming behaviour of white sharks (Carcharodon carcharias) in Australian waters. Mar Biol 150:161–172. doi:10.1007/s00227-006-0325-1

    Article  Google Scholar 

  • Castro ALF, Stewart BS, Wilson SG, Hueter RE, Meekan MG, Motta PJ (2007) Population genetic structure of earth’s largest fish, the whale shark (Rhincodon typus). Mol Ecol 16:5183–5192. doi:10.1111/j.1365-294X.2007.03597.x

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Daly-Engel TS, Grubbs RD, Feldheim KA, Bowen BW, Toonen RJ (2010) Is multiple mating beneficial or unavoidable? Low multiple paternity and genetic diversity in the shortspine spurdog Squalus mitsukurii. Mar Ecol Prog Ser 403:255–267. doi:10.3354/meps08417

    Article  CAS  Google Scholar 

  • DiBattista JD, Feldheim KA, Gruber SH, Hendry AP (2008) Are indirect genetic benefits associated with polyandry? Testing predictions in a natural population of lemon sharks. Mol Ecol 17:783–795. doi:10.1111/j.1365-294X.2007.03623.x

    Article  Google Scholar 

  • Dudgeon CL, Broderick D, Ovenden JR (2009) IUCN classification zones concord with, but underestimate, the population genetic structure of the zebra shark Stegostoma fasciatum in the Indo-West Pacific. Mol Ecol 18:248–261. doi:10.1111/j.1365-294X.2008.04025.x

    Article  CAS  Google Scholar 

  • Duncan KM, Martin AP, Bowen BW, de Couet HG (2006) Global phylogeography of the scalloped hammerhead Sphyrna lewini. Mol Ecol 15:2239–2251. doi:10.1111/j.1365-294X.2006.02933.x

    Article  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arelquin version 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  Google Scholar 

  • Feldheim KA, Gruber SH, Ashley MV (2001) Population genetic structure of the lemon shark (Negaprion brevirostris) in the western Atlantic: DNA microsatellite variation. Mol Ecol 10:295–303

    Article  CAS  Google Scholar 

  • Feldheim KA, Gruber SH, Ashley MV (2002) The breeding biology of lemon sharks at a tropical nursery lagoon. Proc R Soc Biol Sci Lond Ser B 269:1655–1661

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • Goudet J (2002) Fstat, a program to estimate and test gene diversities and fixation indices (version 2.9.3.2). Available from http://www2.unil.ch/popgen/softwares/fstat.htm

  • Grant WS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardine and anchovies and lessons for conservation. J Hered 89:415–426

    Article  Google Scholar 

  • Gu X, Zhang J (1997) A simple method for estimating the parameter of substitution rate variation among sites. Mol Biol Evol 14:1106–1113

    CAS  Google Scholar 

  • Hailer F, Helander B, Folkestad AO et al (2006) Bottlenecked but long-lived: high genetic diversity retained in white-tailed eagles upon recovery from population decline. Biol Lett 2:316–319. doi:10.1098/rsbl.2006.0453

    Article  Google Scholar 

  • Hauser L, Adcock GJ, Smith PJ, Bernal Ramirez JH, Carvalho GR (2002) Loss of microsatellite diversity and low effective population size in an overexploited population of New Zealand snapper (Pagrus auratus). Proc Natl Acad Sci 99:11742–11747. doi:10.1073/pnas.172242899

    Article  CAS  Google Scholar 

  • Hoelzel AR, Shivji MS, Magnussen J, Francis MP (2006) Low worldwide genetic diversity in the basking shark (Cetorhinus maximus). Biol Lett 2:639–642. doi:10.1098/rsbl.2006.0513

    Article  CAS  Google Scholar 

  • Hueter RE, Heupel MR, Heist EJ, Keeney DB (2004) Evidence of philopatry in sharks and implications for the management of shark fisheries. J Northw Atl Fish Sci 35:239–247

    Article  Google Scholar 

  • Jenkins DG, Brescacin CR, Duxbury CV et al (2007) Does size matter for dispersal distance? Glob Ecol Biogeogr 16:415–425. doi:10.1111/j.1466-8238.2007.00312.x

    Article  Google Scholar 

  • Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026. doi:10.1111/j.1365-294X.2008.03887.x

    Article  Google Scholar 

  • 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 15:3669–3679. doi:10.1111/j.1365-294X.2006.03036.x

    Article  CAS  Google Scholar 

  • Keeney DB, Heupel MR, Hueter RC, Heist EJ (2005) Microsatellite and mitochondrial DNA analyses of genetic structure of blacktip shark (Carcharhinus limbatus) nurseries in the northwestern Atlantic, Gulf of Mexico, and Caribbean Sea. Mol Ecol 14:1911–1923. doi:10.1111/j.1365-294X.2005.02549.x

    Article  CAS  Google Scholar 

  • Last PR, Stevens JD (2009) Sharks and rays of Australia, 2nd edn. CSIRO Division of Fisheries, Melbourne

    Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinforma 25:1451–1452. doi:10.1093/bioinformatics/btp187

    Article  CAS  Google Scholar 

  • Lippe C, Dumont P, Bernatchez L (2006) High genetic diversity and no inbreeding in the endangered copper redhorse, Moxostoma hubbsi (Catostomidae, Pisces): the positive sides of a long generation time. Mol Ecol 15:1769–1780. doi:10.1111/j.1365-294X.2006.02902.x

    Article  CAS  Google Scholar 

  • 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. doi:10.1111/j.1365-294X.2007.03392.x

    Article  CAS  Google Scholar 

  • Martin AP (1995) Mitochondrial DNA sequence evolution in sharks—rates, patterns, and phylogenetic inferences. Mol Biol Evol 12:114–1123

    CAS  Google Scholar 

  • Martin RA (2005) Conservation of freshwater and euryhaline elasmobranchs: a review. J Mar Biol Assoc UK 85:1049–1073

    Article  Google Scholar 

  • Meirmans PG (2006) Using the AMOVA framework to estimate a standardised genetic differentiation measure. Evolution 60:2399–2402. doi:10.1111/j.0014-3820.2006.tb01874.x

    Google Scholar 

  • Musick JA, Grubbs RD, Baum J, Cortés E (2007) Carcharhinus obscurus. In: IUCN 2010. IUCN Red List of Threatened Species Version 2010.3. http://www.iucnredlist.org. Accessed 21 Aug 2010

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

    Google Scholar 

  • Non AL, Kitchen A, Mulligan CJ (2007) Identification of the most informative regions of the mitochondrial genome for phylogenetic and coalescent analyses. Mol Phylogenet Evol 44:1164–1171. doi:10.1016/j.ympev.2006.12.020

    Article  CAS  Google Scholar 

  • Nylander JAA (2004) MrAIC.pl. Program distributed by the author. Evolutionary Biology Centre, Uppsala University

  • Otway NM, Bradshaw CJA, Harcourt RG (2004) Estimating the rate of quasi-extinction of the Australian grey nurse shark (Carcharias taurus) population using deterministic age- and stage-classified models. Biol Conserv 119:341–350. doi:10.1016/j.biocon.2003.11.017

    Article  Google Scholar 

  • 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 9:40–54. doi:10.1186/1471-2148-9-40

    Article  Google Scholar 

  • Palsbøll PJ, Bérubé M, Allendorf F (2007) Identification of management units using population genetic data. Trends Ecol Evol 22:11–16

    Article  Google Scholar 

  • Pardini AT, Jones CS, Noble LR, Kreiser B, Malcom H, Bruce BD, Stevens JD, Cliff G, Scholl MC, Francis M, Duffy CAJ, Martin AP (2001) Sex-biased dispersal in great white sharks. Nature 412:139–140

    Article  CAS  Google Scholar 

  • Peverell SC (2005) Distribution of sawfishes (Pristidae) in the Queensland Gulf of Carpentaria, Australia, with notes on sawfish ecology. Environ Biol Fish 73:391–402. doi:10.1007/s-10641-005-1599-8

    Article  Google Scholar 

  • Peverell SC (2008) Sawfish (Pristidae) of the Gulf of Carpentaria, Queensland Australia. Master thesis, James Cook University

  • Phillips N, Chaplin J, Morgan D, Peverell S (2009) Extraction and amplification of DNA from the dried rostra of sawfishes (Pristidae) for applications in conservation genetics. Pac Conserv Biol 15:128–134

    Google Scholar 

  • Plank SM, Lowe CG, Feldheim KA, Wilson RR, Brusslan JA (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. doi:10.1111/j.1095-8649.2010.02677.x

    Article  CAS  Google Scholar 

  • Pogonoski JJ, Pollard DA, Paxton JR (2002) Conservation overview and action plan for Australian threatened and potentially threatened marine and estuarine fishes. Environment Australia, Canberra

    Google Scholar 

  • 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. doi:10.1111/j.1365-294X.2010.04626.x

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283

    Article  Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    CAS  Google Scholar 

  • Schluessel V, Broderick D, Collin SP, Ovenden JR (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. doi:10.1111/j.1469-7998.2009.00680.x

    Google Scholar 

  • 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. doi:10.1111/j.1365-294X.2008.04000.x

    Article  CAS  Google Scholar 

  • Simpfendorfer CA (2000) Predicting population recovery rates for endangered western Atlantic sawfishes using demographic analysis. Environ Biol Fish 58:371–377

    Article  Google Scholar 

  • Simpfendorfer CA (2002) Smalltooth sawfish: the USA’s first endangered elasmobranch? Mar Mat 19:45–49

    Google Scholar 

  • Stabell OB (1984) Homing and olfaction in salmonids: a critical review of with special references to the Atlantic salmon. Biol Rev Camb Philos Soc 59:333–388. doi:10.1111/j.1469-185x.1984.tb00709.x

    Article  CAS  Google Scholar 

  • Stevens JD, Bonfil R, Dulvy NK, Walker PA (2000) The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES J Mar Sci 57:476–494. doi:10.1006/jmsc.2000.0724

    Article  Google Scholar 

  • Stewart BS, Wilson SG (2005) Threatened fishes of the world: Rhincodon typus (Smith 1828) (Rhincodontidae). Environ Biol Fish 74:184–185. doi:10.1007/s10641-005-2229-1

    Article  Google Scholar 

  • Stow A, Zenger K, Briscoe D, Gillings M, Peddemors V, Otway N, Harcourt R (2006) Isolation and genetic diversity of endangered grey nurse shark (Carcharias taurus) populations. Biol Lett 2:308–311. doi:10.1007/s-10641-005-1599-8

    Article  Google Scholar 

  • Swart MKJ, Ferguson JWH, du Toit R, Flamand JRB (1994) Substantial genetic variation in Southern African Black Rhinoceros (Diceros bicornis). J Hered 85:261–266

    CAS  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  Google Scholar 

  • Takagi M (2003) Philopatry and habitat selection in Bull-headed and Brown shrikes. J Field Ornithol 74:45–52

    Google Scholar 

  • 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 10:512–526

    CAS  Google Scholar 

  • Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633

    CAS  Google Scholar 

  • Thorburn DC, Peverell S, Stevens JD, Last PR, Rowland AJ (2003) Status of freshwater and estuarine elasmobranchs in northern Australia. Report to the Natural Heritage Trust, Australia

  • Thorburn DC, Morgan DL, Rowland AJ, Gill HS (2007) Freshwater Sawfish Pristis microdon Latham, 1794 (Chondrichthyes: Pristidae) in the Kimberley region of Western Australia. Zootaxa 1471:27–41

    Google Scholar 

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

    Article  Google Scholar 

  • Ward RD (2006) The importance of identifying spatial population structure in restocking and stock enhancement programmes. Fish Res 80:9–18. doi:10.1016/j.fishres.2006.03.009

    Article  Google Scholar 

  • Watabe S (1991) Electrophoretic analyses of freshwater elasmobranchs from northern Australia and Papua New Guinea. Nat Cult 3:103–109

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • White WT, Kyne PM (2010) The status of chondrichthyan conservation in the Indo-Australasian region. J Fish Biol 76:2090–2117. doi:10.1111/j.1095-8649.2010.02654.x

    Article  CAS  Google Scholar 

  • White TA, Stefanni S, Stamford J, Hoelzel AR (2009) Unexpected panmixia in a long-lived, deep-sea fish with well-define spawning habitat and relatively low fecundity. Mol Ecol 18:2563–2573. doi:10.1111/j.1365-294X.2009.04218.x

    Article  Google Scholar 

  • Whitty JM, Morgan DL, Peverell SC, Thorburn DC (2009) Ontogenetic depth partitioning by juvenile freshwater sawfish (Pristis microdon: Pristidae) in a riverine environment. Mar Fresh Res 60:306–316

    Article  Google Scholar 

  • Wishart DS, Stothard P, Van Domselaar GH (2000) PepTool and GeneTool: platform-independent tools for biological sequence analysis. Methods Mol Biol 132:93–113

    CAS  Google Scholar 

Download references

Acknowledgments

This study was funded by the Australian Government Department of the Environment, Water, Heritage and the Arts and Murdoch University. Thank you to all of the people who donated tissue samples. Thanks also to the Western Australian Department of Fisheries (Rory McAuley and Justin Chidlow), Cairns Marine (Lyle Squire Jnr), Northern Territory Department of Fisheries (Grant Johnson), the Museum and Art Gallery of the Northern Territory (Helen Larson), the Western Australian Museum (Glenn Moore and Sue Morrison), the Australian National Museum (Jeff Johnson), and the Australian Institute of Marine Science (Iain Field). Thank you also to all the people who provided assistance in sample collection including Jeff Whitty, James Tweedley, Dean Thorburn, Simon Visser, Jenny Giles, and William White. We would also like to thank the Yiriman Rangers including, Travis Fazeldean, Cannie, Nyaburu and Kimberley Watson, Josh Albert and Simon Keenan for help with sample collections. Lastly, we would like to thank Michelle Gardner, Glenn Moore, and the anonymous reviewers for comments and suggestions that have improved the quality of this manuscript.

Author information

Authors and Affiliations

  1. Centre for Fish and Fisheries Research, Murdoch University, South Street, Murdoch, WA, 6150, Australia

    Nicole M. Phillips, Jennifer A. Chaplin & David L. Morgan

  2. Queensland Department of Primary Industries and Fisheries, Sustainable Fisheries, Northern Fisheries Centre, Cairns, QLD, 4870, Australia

    Stirling C. Peverell

Authors
  1. Nicole M. Phillips
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jennifer A. Chaplin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David L. Morgan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stirling C. Peverell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nicole M. Phillips.

Additional information

Communicated by M. I. Taylor.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 129 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Phillips, N.M., Chaplin, J.A., Morgan, D.L. et al. Population genetic structure and genetic diversity of three critically endangered Pristis sawfishes in Australian waters. Mar Biol 158, 903–915 (2011). https://doi.org/10.1007/s00227-010-1617-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-010-1617-z

Keywords

Search

Navigation