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Phylogeography of Leiopelma hochstetteri reveals strong genetic structure and suggests new conservation priorities

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Abstract

Leiopelma hochstetteri belongs to a singular anuran lineage endemic to New Zealand that diverged from other frogs about 200 million years ago. The species now is reduced to a series of isolated populations in the northern half of the North Island and Great Barrier Island. We have used mitochondrial and nuclear sequence data to examine the genetic affinities of extant populations of L. hochstetteri. Phylogenetic reconstructions reveal that populations are highly structured. Each of the geographically isolated populations harbours independent mtDNA lineages as well as different degrees of nuDNA differentiation. Moreover, molecular dating reveals that this structure originated in the early Pleistocene. This pattern of genetic structure likely results from unfavourable climatic conditions during the Pleistocene combined with the low dispersal ability of the species. Isolated populations in forested refugia existed even in the southern part of the distribution of the species during glacial cycles. Previously published variation in chromosome numbers and isozyme data are consistent with the new evidence. We identified 13 evolutionary significant units (ESUs) that should serve as the focus for future management and conservation of this species.

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References

  • Abdelkrim J, Robertson BC, Stanton JL, Gemmell NJ (2009) Fast, cost-effective development of species-specific microsatellite markers by genomic sequencing. Biotechniques 46:185–192

    Article  CAS  PubMed  Google Scholar 

  • Akaike H (1974) A new look at the statistical model identification. Inst Electr Electron Engin Trans Autom Contr 19(6):716–723

    Article  Google Scholar 

  • Apte S, Smith PJ, Wallis GP (2007) Mitochondrial phylogeography of New Zealand freshwater crayfishes, Paranephrops spp. Mol Ecol 16:1897–1908. doi:10.1111/j.1365-294X.2007.03224.x

    Article  CAS  PubMed  Google Scholar 

  • Avise JC (1994) Molecular markers, natural history and evolution. Chapman and Hall, New York 511 pp

    Google Scholar 

  • Baber M, Moulton H, Kennedy CS, Gemmell NJ, Crossland M (2006) Discovery, genetic status, and spatial assessment of a Hochstetter’s frog (Leiopelma hochstetteri) population found in Maungatautari Scenic Reserve, New Zealand. N Z J Zool 33:147–156

    Google Scholar 

  • Bell BD (1985) Conservation status of the endemic New Zealand frogs. In: Grigg G, Shine R, Ehmann H (eds) The biology of Australasian frogs and reptiles. Surrey Beatty and Sons, Chipping Norton, pp 449–458

    Google Scholar 

  • Bell BD (1994) A review of the status of New Zealand Leiopelma species (Anura: Leiopelmatidae), including a summary of demographic studies in Coromandel and on Maud Island. N Z J Zool 21:341–349

    Google Scholar 

  • Bell B, Tocher M, Bishop P, Waldman B (2004) Leiopelma hochstetteri. In: IUCN 2007. 2007 IUCN Red List of Threatened Species. www.iucnredlist.org. Downloaded on 05 October 2008

  • Bossuyt F, Milinkovitch MC (2000) Convergent adaptive radiations in Madagascan and Asian ranid frogs reveal covariation between larval and adult traits. Proc Natl Acad Sci USA 97:6585–6590. doi:10.1073/pnas.97.12.6585

    Article  CAS  PubMed  Google Scholar 

  • Bowsher JH (2000) Intraspecific variation in New Zealand’s endemic frog Leiopelma hochstetteri. M.Sc. Thesis, University of Canterbury, New Zealand

  • Buschiazzo E, Gemmell NJ (2006) The rise, fall and renaissance of microsatellites in eukaryotic genomes. Bioessays 28:1040–1050. doi:10.1002/bies.20470

    Article  CAS  PubMed  Google Scholar 

  • Chapple DG, Daugherty CH, Ritchie PA (2008) Comparative phylogeography reveals pre-decline population structure of New Zealand Cyclodina (Reptilia: Scincidae) species. Biol J Linn Soc Lond 95:388–408. doi:10.1111/j.1095-8312.2008.01062.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 

  • Daugherty CH, Patterson GB, Hitchmough RA (1994) Taxonomic and conservation review of the New Zealand herpetofauna. N Z J Zool 21:317–323

    Google Scholar 

  • Didham RK, Ewers RM, Gemmell NJ (2005) Comment on “avian extinction and mammalian introductions on oceanic islands”. Science 307:1412a. doi:10.1126/science.1107333

    Article  Google Scholar 

  • Driscoll DA (1998a) 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 

  • Driscoll DA (1998b) Genetic structure of the frogs Geocrinia lutea and G. rosea reflects extreme population divergence and range changes, not dispersal barriers. Evol Int J Org Evol 52:1147–1157. doi:10.2307/2411244

    Google Scholar 

  • Drost F, Renwick J, Bhaskaran B, Oliver H, McGregor J (2007) A simulation of New Zealand’s climate during the last glacial maximum. Quat Sci Rev 26:2505–2525. doi:10.1016/j.quascirev.2007.06.005

    Article  Google Scholar 

  • Efron B (1979) 1977 Rietz lecture—bootstrap methods—another look at the jackknife. Ann Stat 7:1–26. doi:10.1214/aos/1176344552

    Article  Google Scholar 

  • Estes R, Reig OA (1973) The early fossil record of frogs: a review of the evidence. In: Vial JL (ed) Evolutionary biology of the Anurans: contemporary research on major problems. University of Missouri Press, Columbia, pp 11–63

    Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evol Int J Org Evol 39:783–791. doi:10.2307/2408678

    Google Scholar 

  • Fitzinger LJ (1861) Eine neue Batrachier–Gattung aus Neu–Seeland. Verh Zoologisch-Botanischen Ges 2:217

    Google Scholar 

  • Fouquet A, Gilles A, Vences M, Marty C, Blanc M, Gemmell NJ (2007) Underestimation of species richness in neotropical frogs revealed by mtDNA analyses. PLoS ONE 2:e1109. doi:10.1371/journal.pone.0001109

    Article  PubMed  Google Scholar 

  • Gardner RC, de Lange P, Keeling DJ, Bowala T, Brown HA, Wright SD (2004) A late quaternary phylogeography for Metrosideros (Myrtaceae) in New Zealand inferred from chloroplast DNA haplotypes. Biol J Linn Soc Lond 83:399–412. doi:10.1111/j.1095-8312.2004.00398.x

    Article  Google Scholar 

  • Green DM (1994) Genetic and cytogenetic diversity in Hochstetter’s frog, Leiopelma hochstetteri, and its importance for conservation management. N Z J Zool 21:417–424

    Google Scholar 

  • Green DM, Tessier C (1990) Distribution and abundance of Hochstetter’s frog, Leiopelma hochstetteri. J R Soc N Z 20:261–268

    Google Scholar 

  • Green DM, Zeyl C, Sharbel TF (1993) The evolution of hypervariable sex and supernumerary chromosomes in the relict New Zealand frog, Leiopelma hochstetteri. J Evol Biol 6:417–441. doi:10.1046/j.1420-9101.1993.6030417.x

    Article  Google Scholar 

  • Healy J (1992) Central volcanic region. In: Soons JM, Selby MJ (eds) Landforms of New Zealand. Longman Paul Ltd., Hong Kong, pp 256–286

    Google Scholar 

  • Hey J, Nielsen R (2007) Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc Natl Acad Sci USA 104:2785–2790. doi:10.1073/pnas.0611164104

    Article  CAS  PubMed  Google Scholar 

  • Hitchmough R (2002) New Zealand threat classification system lists. Threatened species occasional publication 23. Department of Conservation, Wellington

    Google Scholar 

  • Holyoake A, Waldman B, Gemmell NJ (2001) Determining the species status of one of the world’s rarest frogs: a conservation dilemma. Anim Conserv 4:29–36. doi:10.1017/S1367943001001032

    Article  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17:754–755. doi:10.1093/bioinformatics/17.8.754

    Article  CAS  PubMed  Google Scholar 

  • James CH, Moritz C (2000) Intraspecific phylogeography in the sedge frog Litoria fallax (Hylidae) indicates pre-Pleistocene vicariance of an open forest species from eastern Australia. Mol Ecol 9:349–358. doi:10.1046/j.1365-294x.2000.00885.x

    Article  CAS  PubMed  Google Scholar 

  • Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13. v.3.15 http://ibdws.sdsu.edu/

  • Knowles LL, Carstens BC (2007) Delimiting species without monophyletic gene trees. Syst Biol 56:887–895. doi:10.1080/10635150701701091

    Article  PubMed  Google Scholar 

  • Lloyd BD (2003a) Intraspecific phylogeny of the New Zealand short-tailed bat Mystacina tuberculata inferred from multiple mitochondrial gene sequences. Syst Biol 52(4):460–476. doi:10.1080/10635150390218187

    Article  PubMed  Google Scholar 

  • Lloyd BD (2003b) Demographic history of the New Zealand short-tailed bat Mystacina tuberculata inferred from modified control region sequences. Mol Ecol 12:1895–1911. doi:10.1046/j.1365-294X.2003.01879.x

    Article  PubMed  Google Scholar 

  • Maddison WP (1997) Gene trees in species trees. Syst Biol 46:523–536. doi:10.2307/2413694

    Google Scholar 

  • McGlone MS (1988) New Zealand. In: Huntley B, Webb TIII (eds) Handbook of vegetation science, vegetation history. Kluwer Academic Publishers, Dordrecht, pp 558–599

    Google Scholar 

  • McGlone MS, Salinger MJ, Moar NT (1993) Paleovegetation studies of New Zealand’s climate since the last glacial maximum. In: Wright HE, Kutzbach JE, Webb T, Ruddiman WF, Street-Perrot JA, Bartlein PJ (eds) Global climates since the last glacial maximum. University of Minnesota Press, MN, pp 294–317

    Google Scholar 

  • McGlone MS, Duncan RP, Heenan PB (2001) Endemism, species selection and the origin and distribution of the vascular plants of New Zealand. J Biogeogr 28:199–216. doi:10.1046/j.1365-2699.2001.00525.x

    Article  Google Scholar 

  • Molloy J, Bell B, Clout M, de Lange P, Gobbs G, Given D, Norton D, Smith N, Stephens T (2002) Classifying species according to threat of extinction—a system for New Zealand. Threatened species occasional publication 22. Department of Conservation, Wellington

    Google Scholar 

  • Morgan-Richards M (1997) Intraspecific karyotype variation is not concordant with allozyme variation in the Auckland tree weta of New Zealand, Hemideina thoracica (Orthoptera: Stenopelmatidae). Biol J Linn Soc Lond 60:423–442

    Google Scholar 

  • Moritz C (1994) Defining ‘evolutionarily significant units’ for conservation. Trends Ecol Evol 9:373–375. doi:10.1016/0169-5347(94)90057-4

    Article  Google Scholar 

  • Mueller RL (2006) Evolutionary rates, divergence dates, and the performance of mitochondrial genes in Bayesian phylogenetic analysis. Syst Biol 55:289–300. doi:10.1080/10635150500541672

    Article  PubMed  Google Scholar 

  • Newman D (1996) Native frog (Leiopelma spp.) recovery plan. Threatened species recovery plan no. 18. Department of Conservation, Wellington

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Roelants K, Gower DJ, Wilkinson M, Loader SP, Biju SD, Guillaume K, Moriau L, Bossuyt F (2007) Global patterns of diversification in the history of modern amphibians. Proc Natl Acad Sci USA 104:887–892. doi:10.1073/pnas.0608378104

    Article  CAS  PubMed  Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    CAS  PubMed  Google Scholar 

  • Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497. doi:10.1093/bioinformatics/btg359

    Article  CAS  PubMed  Google Scholar 

  • Ryder OA (1986) Species conservation and systematics: the dilemma of subspecies. Trends Ecol Evol 1:9–10. doi:10.1016/0169-5347(86)90059-5

    Article  Google Scholar 

  • Salducci M-D, Marty C, Fouquet A, Gilles A (2005) Phylogenetic relationships and biodiversity in Hylids (Anura: Hylidae) from French Guiana. C R Biol 328:1009–1024. doi:10.1016/j.crvi.2005.07.005

    Article  CAS  PubMed  Google Scholar 

  • Shaffer G, Fellers GM, Magee A, Voss R (2000) The genetics of amphibian declines: population substructure and molecular differentiation in the Yosemite Toad, Bufo canorus (Anura, Bufonidae) based on single-strand conformation polymorphism analysis (SSCP) and mitochondrial DNA sequence data. Mol Ecol 9:245–257. doi:10.1046/j.1365-294x.2000.00835.x

    Article  CAS  PubMed  Google Scholar 

  • Sparks R, Melhuish W, McKee J, Ogden J, Palmer J, Molloy B (1995) C-14 calibration in the southern hemisphere and the date of the last Taupo eruption: evidence from tree-ring sequences. Radiocarbon 37:155–163

    CAS  Google Scholar 

  • Stephens M, Donnelly P (2003) A comparison of bayesian methods for haplotype reconstruction. Am J Hum Genet 73:1162–1169. doi:10.1086/379378

    Article  CAS  PubMed  Google Scholar 

  • Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989. doi:10.1086/319501

    Article  CAS  PubMed  Google Scholar 

  • Stevens G, McGlone M, McCulloch B (1995) Prehistoric New Zealand. Reed, Auckland

    Google Scholar 

  • Stuart SN, Hoffmann M, Chanson JS, Cox NA, Berridge RJ, Ramani P, Young BE (eds) (2008) Threatened amphibians of the world. Lynx Edicions, Barcelona

    Google Scholar 

  • Swofford D (2000) PAUP: phylogenetic analysis using parsimony. Sinauer Associates, Sunderland

    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 

  • Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA-sequence data. 3. Cladogram estimation. Genetics 132:619–633

    CAS  PubMed  Google Scholar 

  • Tessier C, Slaven D, Green DM (1991) Population density and daily movement patterns of Hochstetter’s frogs, Leiopelma hochstetteri, in a New Zealand mountain stream. Herpetologica 25:213–214. doi:10.2307/1564652

    Article  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. doi:10.1093/nar/25.24.4876

    Article  CAS  PubMed  Google Scholar 

  • Vences M, Wake D (2007) Speciation, species boundaries and phylogeography of amphibians. In: Heatwole H, Tyler M (eds) Amphibian biology, vol. 6, speciation. Surrey Beatty and Sons, Chipping Norton, pp 2613–2669

    Google Scholar 

  • Vences M, Thomas M, Bonett RM, Vieites DR (2005) Deciphering amphibian diversity through DNA barcoding: chances and challenges. Philos Trans R Soc B Biol Sci 360:1859–1868. doi:10.1098/rstb.2005.1717

    Article  CAS  Google Scholar 

  • Waldman B, Tocher M (1998) Behavioral ecology, genetic diversity, and declining amphibian populations. In: Caro T (ed) Behavioral ecology and conservation biology. Oxford University Press, New York, pp 393–443

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Waples RS (1991) Pacific salmon, Oncorhynchus spp., and the definition of a ‘species’ under the Endangered Species Act. Mar Fish Rev 53:11–22

    Google Scholar 

  • White DJ, Wolff JN, Pierson M, Gemmell NJ (2008) Revealing the hidden complexities of mtDNA inheritance. Mol Ecol 17:4925–4942. doi:10.1111/j.1365-294X.2008.03982.x

    Article  CAS  PubMed  Google Scholar 

  • Worthy TH (1987) Palaeoecological information concerning members of the frog genus Leiopelma: Leiopelmatidae in New Zealand. J R Soc N Z 17:409–420

    Google Scholar 

  • Zeisset I, Beebee TJC (2008) Amphibian phylogeography: a model for understanding historical aspects of species distributions. Heredity 101:109–119. doi:10.1038/hdy.2008.30

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Karen Eggers, Andrew Glaser, David King, and John Heaphy for assistance with samples and sample collection. We also thank Sharyn Goldstein for laboratory assistance and help with data analysis. We are in debt of Amanda Haigh who provided useful comments on an early version of this manuscript and Ben Bell who help with essential information about the species as well as three anonymous reviewers and the editor for their comments on the manuscript. All work was undertaken under permits issued by the New Zealand Department of Conservation, and with the approval of the University of Canterbury Animal Ethics Committee. This work was funded from a subcontract to NJG from the Landcare Research OBI “Sustaining and Restoring Biodiversity” (FRST C09X0503).

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Authors and Affiliations

  1. Molecular Ecology Laboratory, School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, New Zealand

    Antoine Fouquet & Julia H. Bowsher

  2. UMR 6116 IMEP, Equipe Persistance et Evolution de la Biodiversité, Case 36, Université de Provence, Centre St Charles, 3 place Victor Hugo, 13331, Marseille, France

    Antoine Fouquet

  3. Redpath Museum, McGill University, 859 Sherbrooke St. W., Montreal, QC, H3A 2K6, Canada

    David M. Green

  4. Department of Ecology, Lincoln University, P.O. Box 84, Canterbury, New Zealand

    Bruce Waldman

  5. Department of Molecular and Cellular Biology, University of Arizona, 1007 E. Lowell St., Tucson, AZ, 85721, USA

    Julia H. Bowsher

  6. SCION (New Zealand Forest Research Institute Ltd), Private Bag 3020, Rotorua, New Zealand

    Katherine P. McBride

  7. Centre for Reproduction and Genomics, Department of Anatomy and Structural Biology, University of Otago, P.O. Box 913, Dunedin, 9054, New Zealand

    Neil J. Gemmell

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  1. Antoine Fouquet
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Correspondence to Antoine Fouquet.

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Fouquet, A., Green, D.M., Waldman, B. et al. Phylogeography of Leiopelma hochstetteri reveals strong genetic structure and suggests new conservation priorities. Conserv Genet 11, 907–919 (2010). https://doi.org/10.1007/s10592-009-9935-8

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