Conservation Genetics

, Volume 17, Issue 5, pp 1067–1079 | Cite as

Phylogeographic-based conservation implications for the New Zealand long-tailed bat, (Chalinolobus tuberculatus): identification of a single ESU and a candidate population for genetic rescue

  • Serena E. DoolEmail author
  • Colin F. J. O’Donnell
  • Joanne M. Monks
  • Sebastien J. Puechmaille
  • Gerald Kerth
Research Article


The New Zealand long-tailed bat (Chalinolobus tuberculatus) is an endemic species threatened with extinction. Since the arrival of humans, massive deforestation has occurred and invasive mammalian predators were introduced. As a result, C. tuberculatus’ distribution shrank dramatically and became fragmented. To aid the management of the remaining populations, two Evolutionary Significant Units (ESUs) were designated: one on each of New Zealand’s main islands. We utilised mitochondrial sequence data (cytb, 703 bp) and 10 nuclear DNA microsatellite loci to reconstruct the demographic history of this species, to characterise the level of genetic diversity in remaining populations, and to assess the current connectivity between them. Our results indicate that the North Island, with the highest genetic diversity, served as a glacial refuge, with a loss of diversity following the path recolonization to the south of the South Island. However, our data are also consistent with continued, or at least very recent, genetic exchange between colonies across the species distribution. The only exception is the Hanging Rock colony on the east coast of the South Island, which appears to be isolated. Thus, there was no support for the previously designated ESUs. Signatures of past population declines were found in three colonies, the most extreme of which was found in Hanging Rock. Consequently, we recommend that it be genetically rescued via translocation from a donor population. In general, future management priorities should treat Chalinolobus tuberculatus as a single unit, focusing on maintaining connectivity between remaining populations, together with continued roost protection and pest control.


Endangered species Chiroptera Bottlenecks Invasive species ESU Genetic rescue Translocation 



We sincerely thank two anonymous reviewers whose comments improved our manuscript. We thank Will Batson, Lucy Bridgman, Iris Broekema, Rhys Burns, Jo Carpenter, Emilie Chavel, Petrina Duncan, Nicola Fullerton, Carly Hill, Sarah Wills, Jono More, Dan Palmer, Tertia Thurley, Jason and Maddie Van de Wetering and Emma Williams for assisting with collecting tissue samples in the field and to Ina Roemer for support in the lab. This study formed part of the Department of Conservation (DOC) Science Investigation 4230 and tissue sampling was conducted under DOC Animal Ethics Committee permits AEC 220 and AEC 234 and using the DOC Tissue Sampling for Bats Standard Operating Procedure.

Supplementary material

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Supplementary material 1 (XLSX 53 kb)
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Supplementary material 2 (FAS 23 kb)
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Supplementary material 3 (DOCX 34 kb)


  1. Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinform 9:323–327. doi: 10.1186/1471-2105-9-323 CrossRefGoogle Scholar
  2. Arbogast BS, Kenagy GJ (2001) Comparative phylogeography as an integrative approach to historical biogeography. J Biogeogr 28:819–825CrossRefGoogle Scholar
  3. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37CrossRefPubMedGoogle Scholar
  4. Beaumont MA (1999) Detecting population expansion and decline using microsatellites. Genetics 153:2013–2029PubMedPubMedCentralGoogle Scholar
  5. Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond B 263:1619–1626CrossRefGoogle Scholar
  6. Bermingham E, Moritz C (1998) Comparative phylogeography: concepts and applications. Mol Ecol 7:367–369CrossRefGoogle Scholar
  7. Brooks SP, Gelman A (1998) General methods for monitoring convergence of iterative simulations. J Comput Gr Stat 7:434–455Google Scholar
  8. Broquet T, Petit EJ (2009) Molecular estimation of dispersal for ecology and population genetics. Annu Rev Ecol Evol Syst 40:193–216. doi: 10.1146/annurev.ecolsys.110308.120324 CrossRefGoogle Scholar
  9. Burland TM, Barratt EM, Beaumont MA, Racey PA (1999) Population genetic structure and gene flow in a gleaning bat, Plecotus auritus. Proc R Soc Lond B 266:975–980CrossRefGoogle Scholar
  10. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772CrossRefPubMedPubMedCentralGoogle Scholar
  11. Dekrout A, Cursons RT, Wilkins RJ (2009) Microsatellite markers for the endemic New Zealand long-tailed bat (Chalinolobus tuberculatus). Mol Ecol Resour 9:616–618CrossRefPubMedGoogle Scholar
  12. Dool SE et al (2013) Phylogeography and postglacial recolonization of Europe by Rhinolophus hipposideros: evidence from multiple genetic markers. Mol Ecol 22:4055–4070. doi: 10.1111/mec.12373 CrossRefPubMedGoogle Scholar
  13. Dool SE et al (2016) Nuclear introns outperform mitochondrial DNA in phylogenetic reconstruction: lessons from horseshoe bats (Rhinolophidae: Chiroptera). Mol Phylogenet Evol 97:196–212. doi: 10.1016/j.ympev.2016.01.003 CrossRefPubMedGoogle Scholar
  14. Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20CrossRefGoogle Scholar
  15. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. doi: 10.1007/s12686-011-9548-7 CrossRefGoogle Scholar
  16. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  17. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567CrossRefPubMedGoogle Scholar
  18. Excoffier L, Smouse PE, Quattra JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedPubMedCentralGoogle Scholar
  19. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedPubMedCentralGoogle Scholar
  20. Fenton MB (1969) Summer activity of Myotis lucifugus (Chiroptera: Vespertilionidae) at hibernacula in Ontario and Quebec. Can J Zool 47:597–602CrossRefGoogle Scholar
  21. Foley NM et al (2015) How and why overcome the impediments to resolution: lessons from rhinolophid and hipposiderid bats. Mol Biol Evol 32:313–333CrossRefPubMedGoogle Scholar
  22. Francis CM, Habersetzer J (1998) Interspecific and intraspecific variation in echolocation call frequency and morphology of horseshoe bats, Rhinolophus and Hipposideros. In: Kunz TH, Racey PA (eds) Bat: biology and conservation. Smithsonian Institution Press, Washington, pp 169–179Google Scholar
  23. Frankham R (2015) Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow. Mol Ecol 24:2610–2618. doi: 10.1111/mec.13139 CrossRefPubMedGoogle Scholar
  24. Frankham R, Ballou JD, Eldridge MD, Lacy RC, Ralls K, Dudash MR, Fenster CB (2011) Predicting the probability of outbreeding depression. Conserv Biol 25:465–475CrossRefPubMedGoogle Scholar
  25. Gardner RC, De Lange PJ, 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 83:399–412CrossRefGoogle Scholar
  26. Gerlach G, Jueterbock A, Kraemer P, Deppermann J, Harmand P (2010) Calculations of population differentiation based on GST and D: forget GST but not all of statistics! Mol Ecol 19:3845–3852CrossRefPubMedGoogle Scholar
  27. Girod C, Vitalis R, Leblois R, Fréville H (2011) Inferring population decline and expansion from microsatellite data: a simulation-based evaluation of the Msvar method. Genetics 188:165–179CrossRefPubMedPubMedCentralGoogle Scholar
  28. Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19CrossRefGoogle Scholar
  29. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version
  30. Guilbert J, Walker M, Greif S, Parsons S (2007) Evidence of homing following translocation of long-tailed bats (Chalinolobus tuberculatus) at Grand Canyon Cave, New Zealand. N Z J Zool 34:239–246CrossRefGoogle Scholar
  31. Guillot G, Mortier F, Estoup A (2005) GENELAND: a computer package for landscape genetics. Mol Ecol Notes 5:712–715CrossRefGoogle Scholar
  32. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704CrossRefPubMedGoogle Scholar
  33. Heled J, Drummond AJ (2010) Bayesian inference of species trees from multilocus data. Mol Biol Evol 27:570–580. doi: 10.1093/molbev/msp274 CrossRefPubMedGoogle Scholar
  34. Hill JE, Daniel MJ (1985) Systematics of the New Zealand short-tailed bat Mystacina Gray, 1843 (Chiroptera: Mystacinadae). Bull Br Mus Nat Hist Zool 48:279–300Google Scholar
  35. Hitchmough R, Bull L, Cromarty P (2007) New Zealand Threat Classification System lists. Science and Technical Publishing, WellingtonGoogle Scholar
  36. Hoekstra HE, Hirschmann RJ, Bundey RA, Insel PA, Crossland JP (2006) A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 313:101–104CrossRefPubMedGoogle Scholar
  37. Holzapfel S, Faville MZ, Gemmill CE (2002) Genetic variation of the endangered holoparasite Dactylanthus taylorii (Balanophoraceae) in New Zealand. J Biogeogr 29:663–676CrossRefGoogle Scholar
  38. Hoofer SR, Van Den Bussche RA (2003) Molecular phylogenetics of the chiropteran family Vespertilionidae. Acta Chiropterol 5(supplement):1–63CrossRefGoogle Scholar
  39. Hyndman RJ, Einbeck J, Wand M (2013) Package ‘hdrcde’ R package version 3Google Scholar
  40. Jakobsson M, Rosenberg N (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801CrossRefPubMedGoogle Scholar
  41. Jeffreys H (1961) Theory of probability, 3rd edn. Oxford University Press, OxfordGoogle Scholar
  42. Jiang T et al (2013) Factors affecting geographic variation in echolocation calls of the endemic Myotis davidii in China. Ethology 119:881–890CrossRefGoogle Scholar
  43. Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. doi: 10.1093/bioinformatics/btn129 CrossRefPubMedGoogle Scholar
  44. Kerth G (2008) Causes and consequences of sociality in bats. Bioscience 58:737–746CrossRefGoogle Scholar
  45. Kerth G, Petit E (2005) Colonization and dispersal in a social species, the Bechstein’s bat (Myotis bechsteinii). Mol Ecol 14:3943–3950CrossRefPubMedGoogle Scholar
  46. Kerth G, Mayer F, König B (2000) Mitochondiral DNA (mtDNA) reveals that female Bechstein’s bats live in closed societies. Mol Ecol 9:793–800CrossRefPubMedGoogle Scholar
  47. Lettink M, Armstrong DP (2003) An introduction to using mark-recapture analysis for monitoring threatened species. Dep Conserv Tech Ser A 28:5–32Google Scholar
  48. Lin A et al (2015) Geographical variation in echolocation vocalizations of the Himalayan leaf-nosed bat: contribution of morphological variation and cultural drift. Oikos 124:364–371CrossRefGoogle Scholar
  49. Lloyd BD (2003a) The demographic history of the New Zealand short-tailed bat Mystacina tuberculata inferred from modified control region sequences. Mol Ecol 12:1895–1911CrossRefPubMedGoogle Scholar
  50. Lloyd BD (2003b) Intraspecific phylogeny of the New Zealand short-tailed bat Mystacina tuberculata inferred from multiple mitochondrial gene sequences. Syst Biol 52:460–476CrossRefPubMedGoogle Scholar
  51. Loader C (1999) Local regression and likelihood, vol 47. Springer, New YorkGoogle Scholar
  52. McGlone MS, Salinger MJ, Moar NT (1993) Paleovegetation studies of New Zealand’s climate since the last glacial maximum Wright, HE, Jr, Kutzbach, JE, Webb:294–317Google Scholar
  53. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858CrossRefPubMedGoogle Scholar
  54. O’Donnell CFJ (2000a) Conservation status and causes of decline of the thratened New Zealand long-tailed bat Chalinolobus tuberculatus (Chiroptera: Vespertilionidae). Mamm Rev 30:89–106CrossRefGoogle Scholar
  55. O’Donnell CFJ (2000b) Cryptic local populations in a temperate rainforest bat Chalinolobus tuberculatus in New Zealand. Anim Conserv 3:287–297CrossRefGoogle Scholar
  56. O’Donnell CFJ (2001a) Home range and use of space by Chalinolobus tuberculatus, a temperate rainforest bat from New Zealand. J Zool 253:253–264CrossRefGoogle Scholar
  57. O’Donnell CFJ (2002) Variability in numbers of long-tailed bats (Chalinolobus tuberculatus) roosting in Grand Canyon Cave, New Zealand: Implications for monitoring population trends. N Z J Zool 29:273–284CrossRefGoogle Scholar
  58. O’Donnell CFJ (2008) Chalinolobus tuberculatus The IUCN Red List of Threatened Species version 2014.3 <Downloaded on 29 May 2015>: e.T4425A10881758.
  59. O’Donnell CFJ (2010) The ecology and conservation of New Zealand bats. In: Fleming TH, Racey PA (eds) Island bats: evolution, ecology and conservation. Chicago University Press, Chicago, pp 460–495Google Scholar
  60. O’Donnell CFJ, Sedgeley JA (1999) Use of roosts by the long-tailed bat, Chalinolobus tuberculatus, in temperate rainforest in New Zealand. J Mammal 80:913–923CrossRefGoogle Scholar
  61. O’Donnell CFJ, Christie JE, Lloyd B, Parsons S, Hitchmough R (2013) Conservation status of New Zealand bats, 2012 New Zealand Threat Classification Series 6Google Scholar
  62. O’Donnell CFJ, Richter S, Dool SE, Monks JM, Kerth G (2016) Genetic diversity is maintained in the endangered New Zealand long-tailed bat (Chalinolobus tuberculatus) despite a closed social structure and regular population crashes. Conserv Genet 17:91–102. doi: 10.1007/s10592-015-0763-8 CrossRefGoogle Scholar
  63. O’Donnell CFJ (2001b) Advances in New Zealand mammalogy 1990–2000: long-tailed bat. J R Soc N Z 31:43–57CrossRefGoogle Scholar
  64. O’Donnell CFJ, Christie JE, Hitchmough RA, Lloyd B, Parsons S (2010) The conservation status of New Zealand bats, 2009 New Zealand. J Zool 37:297–311Google Scholar
  65. Parsons S (1997) Search-phase echolocation calls of the New Zealand lesser short-tailed bat (Mystacina tuberculata) and long-tailed bat (Chalinolobus tuberculatus). Can J Zool 75:1487–1494CrossRefGoogle Scholar
  66. Peery MZ et al (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418CrossRefPubMedGoogle Scholar
  67. Petit E, Excoffier L, Mayer F (1999) No evidence of bottleneck in the postglacial recolonization of Europe by the noctule bat (Nyctalus noctula). Evolution 53:1247–1258CrossRefGoogle Scholar
  68. Plummer M, Best N, Cowles K, Vines K (2006) CODA: Convergence diagnosis and output analysis for MCMC R news 6:7–11Google Scholar
  69. Porter CA, Primus AW, Hoffmann FG, Baker RJ (2010) Karyology of Five Species of Bats (Vespertilionidae, Hipposideridae, and Nycteridae) from Gabon with Comments on the Taxonomy of Glauconycteris Occasional Papers, Museum of Texas Tech UniversityGoogle Scholar
  70. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  71. Pryde MA, O’Donnell CFJ, Barker RJ (2005) Factors influencing survival and long-term population viability of New Zealand long-tailed bats (Chalinolobus tuberculatus): implications for conservation. Biol Conserv 126:175–185. doi: 10.1016/j.biocon.2005.05.006 CrossRefGoogle Scholar
  72. Pryde MA, Lettink M, O’Donnell CFJ (2006) Survivorship in two populations of long-tailed bats (Chalinolobus tuberculatus) in New Zealand. N Z J Zool 33:85–95CrossRefGoogle Scholar
  73. Puechmaille SJ et al (2011) The evolution of sensory divergence in the context of limited gene flow in the bumblebee bat. Nat Commun 2:573CrossRefPubMedPubMedCentralGoogle Scholar
  74. Puechmaille SJ et al (2012) Genetic analyses reveal further cryptic lineages within the Myotis nattereri species complex. Mammal Biol Zeitschrift für Säugetierkunde 77:224–228. doi: 10.1016/j.mambio.2011.11.004 CrossRefGoogle Scholar
  75. Pujolar J, Bevacqua D, Capoccioni F, Ciccotti E, De Leo G, Zane L (2011) No apparent genetic bottleneck in the demographically declining European eel using molecular genetics and forward-time simulations. Conserv Genet 12:813–825CrossRefGoogle Scholar
  76. Rambaut A, Drummond A (2007) Tracer v1.4 MCMC Trace Analysis Package, Institute of Evolutionary Biology University of Edinburgh (Scotland) & Department of Computer Science University of Auckland (New Zealand) (2003–2007),
  77. Razgour O, Hanmer J, Jones G (2011) Using multi-scale modelling to predict habitat suitability for species of conservation concern: the grey long-eared bat as a case study. Biol Conserv 144:2922–2930. doi: 10.1016/j.biocon.2011.08.010 CrossRefGoogle Scholar
  78. Razgour O et al (2014) Scale-dependent effects of landscape variables on gene flow and population structure in bats. Divers Distrib 20:1173–1185CrossRefGoogle Scholar
  79. Reiter G (2004) The importance of woodland for Rhinolophus hipposideros (Chiroptera, Rhinolophidae) in Austria. Mammalia 68:403–410CrossRefGoogle Scholar
  80. Roehrs ZP, Lack JB, Van Den Bussche RA (2010) Tribal phylogenetic relationships within Vespertilioninae (Chiroptera: Vespertilionidae) based on mitochondrial and nuclear sequence data. J Mammal 91:1073–1092CrossRefGoogle Scholar
  81. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  82. Sedgeley JA, O’Donnell CFJ (2004) Roost use by long-tailed bats in South Canterbury: Testing predictions of roost site selection in a highly fragmented landscape. N Z J Ecol 28:1–18Google Scholar
  83. Simmons NB (2005) Order Chiroptera. In: Wilson DE, Reeder DM (eds) Mammal Species of the World: a taxonomic and geographic reference, 3rd edn. Johns Hopkins University Press, Baltimore, pp 312–529Google Scholar
  84. Spong G, Hellborg L (2002) A near-extinction event in lynx: do microsatellite data tell the tale? Conservation Ecology 6:article 6Google Scholar
  85. Storz JF, Beaumont MA (2002) Testing for genetic evidence of population expansion and contraction: an empirical analysis of microsatellite DNA variation using a hierarchical Bayesian model. Evolution 56:154–166CrossRefGoogle Scholar
  86. Tournant P, Afonso E, Roué S, Giraudoux P, Foltête J-C (2013) Evaluating the effect of habitat connectivity on the distribution of lesser horseshoe bat maternity roosts using landscape graphs. Biol Conserv 164:39–49CrossRefGoogle Scholar
  87. Trewick SA (2000) Mitochondrial DNA sequences support allozyme evidence for cryptic radiation of New Zealand Peripatoides (Onychophora). Mol Ecol 9:269–281CrossRefPubMedGoogle Scholar
  88. Van Oosterhout C, Hutchison WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  89. Vander Wal E, Garant D, Festa-Bianchet M, Pelletier F (2013) Evolutionary rescue in vertebrates: evidence, applications and uncertainty. Philos Trans R Soc B Biol Sci 368:20120090CrossRefGoogle Scholar
  90. Wallis GP, Trewick SA (2009) New Zealand phylogeography: evolution on a small continent. Mol Ecol 18:3548–3580CrossRefPubMedGoogle Scholar
  91. Waters JM, Craw D (2006) Goodbye Gondwana? New Zealand biogeography, geology, and the problem of circularity. Syst Biol 55:351–356CrossRefPubMedGoogle Scholar
  92. Weyeneth N, Goodman SM, Stanley WT, Ruedi M (2008) The biogeography of Miniopterus bats (Chiroptera: Miniopteridae) from the Comoro Archipelago inferred from mitochondrial DNA. Mol Ecol 17:5205–5219. doi: 10.1111/j.1365-294X.2008.03994.x CrossRefPubMedGoogle Scholar
  93. Winnington A (1999) Ecology, genetics and taxonomy of peka peka (Chiroptera: Mystacina tuberculata and Chalinolobus tuberculatus). University of Otago, unpublished Ph.D. thesisGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Serena E. Dool
    • 1
    Email author
  • Colin F. J. O’Donnell
    • 2
  • Joanne M. Monks
    • 3
  • Sebastien J. Puechmaille
    • 1
  • Gerald Kerth
    • 1
  1. 1.Zoological Institute and MuseumGreifswald UniversityGreifswaldGermany
  2. 2.Science and Capability Group, Department of ConservationChristchurchNew Zealand
  3. 3.Science and Capability Group, Department of ConservationDunedinNew Zealand

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