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Evolution and maintenance of divergent lineages in an endangered freshwater fish, Macquaria australasica

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Abstract

Variable hydrological regimes and habitat availability are factors that affect the distribution of freshwater dependent species and are expected to influence their levels of genetic diversity. Although geologically relatively stable, the south eastern region of Australia has experienced significant changes in hydrological conditions during the Quaternary. This area has also been recently affected by anthropogenic activities, resulting in dramatic population declines of Macquarie Perch (Macquaria australasica). We conducted a range-wide phylogeographic study of this endangered fish to assess the relationship between landscape and freshwater fish evolution in south eastern Australia and infer levels of genetic diversity and population structure. Surprisingly, we detected high genetic diversity, with 46 mtDNA control region haplotypes found across 37 sampling locations. Some lineages were remarkably divergent; one represents a putative undescribed species that probably went extinct during the period of this study. Our reconstruction of population history using a combination of coalescent and phylogenetic methods indicates that the species originated on the coast, east of the Great Dividing Range (GDR), with subsequent colonisation of the Murray-Darling basin, west of the GDR. Nested clade and IM analyses inferred a series of range expansions and fragmentations across the species range consistent with the history of climatic oscillations in south eastern Australia during the Pleistocene. We conclude that the unexpected high levels of diversity and divergence observed in M. australasica may be due to specific habitat requirements, localised recruitment, and Pleistocene climate fluctuations. Under expectations of a drier climate and increased sea levels due to global warming, populations of this and other freshwater species may be expected to experience increased habitat fragmentation and loss of genetic diversity. Conservation management should focus on habitat protection, the maintenance of genetic diversity and taxonomic review.

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References

  • Allen G, Midgley S, Allen M (2002) Field guide to the freshwater fishes of Australia. Western Australian Museum, Perth

    Google Scholar 

  • Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622. doi:10.1016/S0169-5347(01)02290-X

    Article  Google Scholar 

  • Appleford P, Anderson TA, Gooley GJ (1998) Reproductive cycle and gonadal development of Macquarie perch Macquaria australasica Cuvier (Percichthyidae), in Lake Dartmouth and tributaries of the Murray-Darling Basin, Victoria, Australia. Mar Freshw Res 49:163–169. doi:10.1071/MF97012

    Article  Google Scholar 

  • Baker AM, Hughes J, Dean JC, Bunn SE (2004) Mitochondrial DNA reveals phylogenetic structuring and cryptic diversity in Australian freshwater macroinvertebrate assemblages. Mar Freshw Res 55:629–640. doi:10.1071/MF04050

    Article  CAS  Google Scholar 

  • Beheregaray LB (2008) Twenty years of phylogeography: the state of the field and the challenges for the southern hemisphere. Mol Ecol 17:3754–3774

    PubMed  Google Scholar 

  • Beheregaray LB, Sunnucks P (2001) Fine-scale genetic structure, estuarine colonization and incipient speciation in the marine silverside fish Odontesthes argentinensis. Mol Ecol 10:2849–2866. doi:10.1046/j.1365-294X.2001.t01-1-01406.x

    Article  CAS  PubMed  Google Scholar 

  • Beheregaray LB, Sunnucks P, Briscoe DA (2002) A rapid fish radiation associated with the last sea-level changes in southern Brazil: the silverside Odontesthes perugiae complex. Proceedings of the Royal Society of London B series 269:65–73

    Article  Google Scholar 

  • Bermingham E, McCafferty SS, Martin AP (1997) Fish biogeography and molecular clocks: perspectives from the Panamanian isthmus. In: Kocher TD, Stepien CA (eds) Molecular systematics of fishes. Academic Press, San Diego, pp 113–126

    Chapter  Google Scholar 

  • Bernatchez L, Wilson CC (1998) Comparative phylogeography of Nearctic and Palearctic fishes. Mol Ecol 7:431–452. doi:10.1046/j.1365-294x.1998.00319.x

    Article  Google Scholar 

  • Bishop P (1982) Stability or change: a review of ideas on ancient drainage in eastern New South Wales. Aust Geogr 15:219–230. doi:10.1080/00049188208702820

    Article  Google Scholar 

  • Bowler J (1990) The last 500, 000 years. In: Mackay N, Eastburn D (eds) The Murray. Murray Darling Basin Commission, Canberra, pp 95–109

    Google Scholar 

  • Bowler JM, Wasson RJ (1983) Glacial age environments of inland Australia. In: SASQUA International Symposium, Swaziland, pp 183–208

  • Bruce A, Knight J, Creese B (2007) Survey of aquatic threatened species Macquarie perch (Macquaria australasica) and Adams’ emerald dragonfly (Archaeophya adamsi) within the Hawkesbury–Nepean catchment. Interim report for the Hawkesbury–Nepean Catchment Management Authority, NSW Department of Primary Industries, Port Stephens Fisheries Centre

  • Cadwallader PL (1978) Some causes of the decline in range and abundance of native fish in the Murray-Darling river system. Proc R Soc Vic 90:211–224

    Google Scholar 

  • Cadwallader PL, Rogan PL (1977) The Macquarie perch, Macquaria australasica (Pisces: Perchichthyidae), of lake Eildon, Victoria. Aust J Ecol 2:409–418. doi:10.1111/j.1442-9993.1977.tb01156.x

    Article  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659. doi:10.1046/j.1365-294x.2000.01020.x

    Article  CAS  PubMed  Google Scholar 

  • Craw D, Burridge CP, Anderson L, Waters JM (2007) Late quaternary river drainage and fish evolution, Southland, New Zealand. Geomorphology 84:98–110. doi:10.1016/j.geomorph.2006.07.008

    Article  Google Scholar 

  • Craw D, Burridge CP, Norris RJ, Water JM (2008) Genetic ages for quaternary topographic evolution: a new dating tool. Geology 36:19–22. doi:10.1130/G24126A.1

    Article  Google Scholar 

  • Crowley LELM, Ivantsoff W, Allen GR (1986) Taxonomic position of two crimson-spotted rainbowfish, Melanotaenia duboulayi and Melanotaenia fluviatilis (Pisces: Melanotaeniidae), from eastern Australia, with special reference to their early life-history stages. Aust J Mar Freshwater Res 37:385–398. doi:10.1071/MF9860385

    Article  Google Scholar 

  • Curry AR (2007) Late glacial impacts on dispersal and colonization of Atlantic Canada and Maine by freshwater fishes. Quat Res 67:225–233. doi:10.1016/j.yqres.2006.11.002

    Article  Google Scholar 

  • Donaldson KA, Wilson RR (1999) Amphi-Panamic geminates of snook (Percoidei: Centropomidae) provide a calibration of the divergence rate in the mitochondrial DNA control region of fishes. Mol Phylogenet Evol 13:208–213. doi:10.1006/mpev.1999.0625

    Article  CAS  PubMed  Google Scholar 

  • Driscoll DA (1998) Genetic structure, metapopulation processes and evolution influence the conservation strategies for two endangered frog species. Biol Conserv 83:43–54. doi:10.1016/S0006-3207(97)00045-1

    Article  Google Scholar 

  • Dufty S (1986) Genetic and morphological divergence between populations of Macquarie perch (Macquaria australasica) east and west of the Great Dividing Range. University of New South Wales, Sydney

    Google Scholar 

  • Durand J-D, Tine M, Panfili J, Thiaw OT, Lae R (2005) Impact of glaciations and geographic distance on the genetic structure of a tropical estuarine fish, Ethmalosa fimbriata (Clupeidae, S. Bowich, 1825). Mol Phylogenet Evol 36:277–287. doi:10.1016/j.ympev.2005.01.019

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2006) Arlequin version 3.1 an integrated software package for population genetics data analysis. University of Geneva, Switzerland

    Google Scholar 

  • Faith D (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10. doi:10.1016/0006-3207(92)91201-3

    Article  Google Scholar 

  • Faulks LK, Gilligan DM, Beheregaray LB (2008) Phylogeography of a threatened freshwater fish (Mogurnda adspersa) in eastern Australia: conservation implications. Mar Freshw Res 59:89–96. doi:10.1071/MF07167

    Article  CAS  Google Scholar 

  • Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508. doi:10.1046/j.1523-1739.1996.10061500.x

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Galloway RW (1965) Late quaternary climates in Australia. J Geol 73:4

    Article  Google Scholar 

  • Garrick RC, Dyer RJ, Beheregaray LB, Sunnucks P (2008) Babies and bathwater: a comment on the premature obituary for nested clade phylogeographical analysis. Mol Ecol 17:1401–1403. doi:10.1111/j.1365-294X.2008.03675.x

    Article  CAS  PubMed  Google Scholar 

  • Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913. doi:10.1038/35016000

    Article  CAS  PubMed  Google Scholar 

  • Hey J, Nielsen R (2004) Multilocus methods for estimating population sizes, migration rates, and divergence time, with application to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747–760. doi:10.1534/genetics.103.024182

    Article  CAS  PubMed  Google Scholar 

  • Ho SYW, Kolokotrinis S-O, Allaby RG (2007) Elevated substitution rates estimated from ancient DNA sequences. Biol Lett 3:702–705. doi:10.1098/rsbl.2007.0377

    Article  CAS  PubMed  Google Scholar 

  • Hughes J, Ponniah M, Hurwood D, Chenoweth SF, Arthington A (1999) Strong genetic structuring in a habitat specialist, the Oxylean pygmy perch Nannoperca oxleyana. Heredity 83:5–14. doi:10.1038/sj.hdy.6885390

    Article  PubMed  Google Scholar 

  • Imbrie J, Hays J, Martinson DG, McIntire A, Mix AC, Morley JJ, Pisias NG, Prell WL, Shackleton NJ (1984) The orbital theory of the Pleistocene climate: support from a revised chronology of the marine δ18O record. In: Berger AL, Imbrie J, Hays J, Kukla G, Salzman B (eds) Milankovitch and climate, part 1. Riedel, Dordrecht, pp 269–305

    Google Scholar 

  • IUCN (2008) 2008 IUCN Red list of threatened species. http://www.iucnredlist.org. Downloaded on 30 Apr 2009

  • Jerry DR (2008) Phylogeography of the freshwater catfish Tandanus tandanus (Plotosidae): a model species to understand evolution of the eastern Australian freshwater fish fauna. Mar Freshw Res 59:351–360. doi:10.1071/MF07187

    Article  Google Scholar 

  • Jerry DR, Elphinstone MS, Baverstock PR (2001) Phylogenetic relationships of Australian members of the family Percichthyidae inferred from mitochondrial 12S rRNA sequence data. Mol Phylogenet Evol 18:335–347. doi:10.1006/mpev.2000.0871

    Article  CAS  PubMed  Google Scholar 

  • Kershaw P, Moss P, Van Der Kaars S (2003) Causes and consequences of long-term climatic variability on the Australian climate. Freshw Biol 48:1274–1283. doi:10.1046/j.1365-2427.2003.01085.x

    Article  Google Scholar 

  • Lake JS (1978) Australian freshwater fishes. Thomas Nelsen Australia, West Melbourne

    Google Scholar 

  • Lee W-J, Conroy J, Howell WH, Kocher TD (1995) Structure and evolution of teleost mitochondrial control regions. J Mol Evol 41:54–66. doi:10.1007/BF00174041

    Article  CAS  PubMed  Google Scholar 

  • Lintermans M (2007) Fishes of the Murray-Darling basin an introductory guide. Murray Darling Basin Commission, Canberra

    Google Scholar 

  • Makinen HS, Merila J (2008) Mitochondrial DNA phylogeography of the three-spined stickleback (Gasterosteus aculeatus) in Europe—evidence for multiple glacial refugia. Mol Phylogenet Evol 46:167–182. doi:10.1016/j.ympev.2007.06.011

    Article  CAS  PubMed  Google Scholar 

  • McClelland EK, Naish KA (2007) What is the fitness outcome of crossing unrelated fish populations? A meta-analysis and an evaluation of future research directions. Conserv Genet 8:397–416. doi:10.1007/s10592-006-9178-x

    Article  Google Scholar 

  • McDowall R (1996) Freshwater fishes of south eastern Australia. Reed Books, Sydney

    Google Scholar 

  • McGlashan DJ, Hughes JM (2001) Genetic evidence for historical continuity between populations of the Australian freshwater fish Craterocephalus stercusmuscarum (Atherinidae) east and west of the Great Dividing Range. J Fish Biol 59:55–67. doi:10.1111/j.1095-8649.2001.tb01378.x

    Article  CAS  Google Scholar 

  • Meehl GA, Stocker TF, Collins WD, Friedlingstein P, Gaye AT, Gregory JM, Kitoh A, Knutti R, Murphy JM, Noda A, Raper SCB, Watterson IG, Weaver AJ, Zhao Z-C (2007) Global climate projections. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Millor HL (ed) Climate change 2007: the physical science basis, contribution of: working group 1 to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 747–846

  • Montgomery ME, Woodworth LM, Nurthen RK, Gilligan DM, Briscoe DA, Frankham R (2000) Relationships between population size and genetic diversity: comparisons of experimental results with theoretical predictions. Conserv Genet 1:33–43. doi:10.1023/A:1010173401557

    Article  CAS  Google Scholar 

  • Moritz C (2002) Strategies to protect diversity and the evolutionary processes that sustain it. Syst Biol 51:238–254. doi:10.1080/10635150252899752

    Article  PubMed  Google Scholar 

  • Musyl MK, Keenan CP (1992) Population genetics and zoogeography of Australian freshwater golden perch, Macquaria ambigua (Richardson 1845) (Teleostei: Percichthyidae), and electrophoretic identification of a new species from the Lake Eyre basin. Aust J Mar Freshwater Res 43:1585–1601. doi:10.1071/MF9921585

    Article  Google Scholar 

  • Musyl MK, Keenan CP (1996) Evidence for cryptic speciation in Australian freshwater eel-tailed catfish, Tandanus tandanus (Teleostei: Plotosidae). Copeia 3:526–534. doi:10.2307/1447516

    Article  Google Scholar 

  • Nott JF, Price DM, Nanson GC (2002) Stream response to quaternary climate change: evidence from the Shoalhaven river catchment, southeastern highlands, temperate Australia. Quat Sci Rev 21:965–974. doi:10.1016/S0277-3791(01)00047-6

    Article  Google Scholar 

  • Ollier CD (1978) Tectonics and geomorphology of the eastern highlands. In: Davies JL, Williams MAJ (eds) Landform evolution in Australasia. Australian National University Press, Canberra, pp 5–48

    Google Scholar 

  • Orr MR, Smith TB (1998) Ecology and speciation. Trends Ecol Evol 13:502. doi:10.1016/S0169-5347(98)01511-0

    Article  Google Scholar 

  • Pels S (1964) The present and ancestral Murray River. Aust Geogr Stud 2:111–119. doi:10.1111/j.1467-8470.1964.tb00029.x

    Article  Google Scholar 

  • Petit RJ (2008) The coup de grâce for the nested clade phylogeographic analysis? Mol Ecol 17:516–518. doi:10.1111/j.1365-294X.2008.03692.x

    Article  PubMed  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818. doi:10.1093/bioinformatics/14.9.817

    Article  CAS  PubMed  Google Scholar 

  • Posada D, Templeton AR (2005) GeoDis revised inference key. Available at http://darwin.uvigo.es/download/geodisKey_11Nov05.pdf. Accessed 7 Feb 2007

  • Posada D, Crandall KA, Templeton AR (2000) GeoDis: a program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Mol Ecol 9:487–488. doi:10.1046/j.1365-294x.2000.00887.x

    Article  CAS  PubMed  Google Scholar 

  • Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109. doi:10.1146/annurev.ecolsys.27.1.83

    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  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) Mr Bayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. doi:10.1093/bioinformatics/btg180

    Article  CAS  PubMed  Google Scholar 

  • Rowland SJ (1993) Maccullochella ikei, an endangered species of freshwater cod (Pisces: Percicthyidae) from the clarence river system, NSW and M. peeli mariensis, a new subspecies from the Mary river system, Qld. Rec Aust Mus 45:121–145

    Google Scholar 

  • State Fisheries NSW (1916) Fisheries: Report on the fisheries of New South Wales for the year 1915. Report to the New South Wales Legislative Assembly, Australia

  • Sunnucks P, Hales DF (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae). Mol Biol Evol 13:510–524

    CAS  PubMed  Google Scholar 

  • Sunnucks P, Wilson AC, Beheregaray LB, Zenger K, French J, Taylor AC (2000) SSCP is not so difficult: the application and utility of single-stranded conformation polymorphism in evolutionary biology and molecular ecology. Mol Ecol 9:1699–1710. doi:10.1046/j.1365-294x.2000.01084.x

    Article  CAS  PubMed  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  PubMed  Google Scholar 

  • Taylor EB, Bentzen P (1993) Evidence for multiple origins and sympatric divergence of trophic ecotypes of smelt (Osmerus) in northeastern North America. Evolution Int J Org Evolution 47:813–832. doi:10.2307/2410186

    Google Scholar 

  • Templeton AR (1998) Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Mol Ecol 7:381–397. doi:10.1046/j.1365-294x.1998.00308.x

    Article  CAS  PubMed  Google Scholar 

  • Wellman P (1979) On the cainozoic uplift of the southeastern Australian highland. J Geol Soc Aust 26:1–9

    Google Scholar 

  • Wright LI, Tregenza T, Hosken DJ (2008) Inbreeding, inbreeding depression and extinction. Conserv Genet 9:833–843. doi:10.1007/s10592-007-9405-0

    Article  Google Scholar 

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Acknowledgments

Samples were provided by the NSW Department of Primary Industries, Arthur Rylah Institute Department of Sustainability and Environment Victoria, the South Australian Museum, and Peter Unmack. Funding for this project was provided by the Australian Research Council (grant LP 0667952 to L. Beheregaray and D. Gilligan) and the New South Wales Department of Primary Industries. We thank Daniel Faith and two anonymous reviewers for their helpful comments.

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Correspondence to Luciano B. Beheregaray.

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Faulks, L.K., Gilligan, D.M. & Beheregaray, L.B. Evolution and maintenance of divergent lineages in an endangered freshwater fish, Macquaria australasica . Conserv Genet 11, 921–934 (2010). https://doi.org/10.1007/s10592-009-9936-7

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