Journal of Mammalian Evolution

, Volume 5, Issue 1, pp 33–64 | Cite as

Affinities and Historical Zoogeography of the New Zealand Short-Tailed Bat, Mystacina tuberculata Gray 1843, Inferred from DNA-Hybridization Comparisons

  • John A. W. Kirsch
  • James M. Hutcheon
  • Deanna G. P. Byrnes
  • Brian D. Lloyd
Article

Abstract

We carried out DNA-hybridization comparisons among representatives of the major groups of Chiroptera to determine the phylogenetic position of the New Zealand short-tailed bat, Mystacina tuberculata. All analyses confirmed the noctilionoid affinity of this species suggested by an earlier serological study, with support from taxon jackknifing and at bootstrap levels of 98% or higher. However, a specific association with Noctilio was not found in more than 13% of the bootstrapped trees. The most precise of the thermal-stability indices employed (Tm, the median melting temperature of hybridized sequences) demonstrated a sister-group relationship of Mystacina to all noctilionoids, with Noctilio the first branch within Noctilionoidea but separated from the Mystacina lineage by a very short internode. Our determination of the timing of the divergence of Mystacina from noctilionoids is 54 myrbp. This estimate is based on independent indications that extant bat lineages began to diversify in the latest Cretaceous and is much earlier than the tentative estimate of 35 myrbp inferred from serology. Even if the diversification of all living bats occurred as early as 83 myrbp, as some authors have suggested, separation of Mystacinidae—on that basis, at 66 myrbp—could not have taken place soon enough for this taxon to be isolated on New Zealand before New Zealand separated from the rest of Gondwanaland. However, any of these dates would allow for the distribution of the noctilionoid–mystacinid common ancestor in South America, Australia, and Antarctica before the final sundering of Australia from Antarctica and for the divergence of Mystacinidae as a possible result of that event. This hypothesis is supported by the presence of fossil mystacinids in early and mid-Miocene deposits at Bullock Creek and Riversleigh, Queensland, showing that Mystacinidae had been resident in Australia from at least 25–20 myrbp. The most obvious scenario explaining the presence of Mystacinidae in New Zealand is therefore fortuitous dispersal from Australia across the Tasman Sea.

bat evolution Chiroptera molecular phylogeny Mystacinidae plate tectonics 

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LITERATURE CITED

  1. Aguilar, J.-P., Calvet, M., Crochet, J.-Y., Legendre, S., Michaux, J., and Sigé, B. (1986). Première occurrence d'un mégachiroptère ptéropodidé dan le Miocène moyen d'Europe (gisement de Lo Fournas-II, Pyrénées-orientales, France). Palaeovertebrata 16: 173–184.Google Scholar
  2. Altringham, J. D. (1996). Bats: Biology and Behaviour, Oxford University Press, Oxford.Google Scholar
  3. Arnason, U., Gullberg, A., and Janke, A. (1997). Phylogenetic analyses of mitochondrial DNA suggests a sister group relationship between Xenarthra (Edentata) and ferungulates. Mol. Biol. Evol. 14: 762–768.Google Scholar
  4. Baillie, J., and Groomridge, B. (1996). IUCN Red List of Threatened Animals, IUCN, The World Conservation Union.Google Scholar
  5. Baker, R. J., Longmire, J. L., Maltbie, M., Hamilton, M. J., and Van Den Bussche, R. A. (1997). DNA synapomorphies for a variety of taxonomic levels from a cosmid library from the New World bat Macrotus waterhousii. Syst. Biol. 46: 579–589.Google Scholar
  6. Beard, K. C., Sigé, B., and Krishtalka, L. (1992). A primitive vespertilionoid bat from the early Eocene of central Wyoming. C.R. Acad. Sci. Paris 314(II): 735–741.Google Scholar
  7. Bleiweiss, R., and Kirsch, J. A. W. (1993). Experimental analysis of variance for DNA hybridization. II. Precision. J. Mol. Evol. 37: 514–524.Google Scholar
  8. Bleiweiss, R., Kirsch, J. A. W., and Matheus, J. C. (1994). DNA hybridization evidence for subfamily structure among hummingbirds. Auk 111: 8–19.Google Scholar
  9. Bonaparte, J. E. (1990). New Late Cretaceous mammals from the Los Alamitos Formation, northern Patagonia. Natl. Geogr. Res. 6(1): 63–93.Google Scholar
  10. Catzeflis, F. M., Sheldon, F. H., Ahlquist, J. E., and Sibley, C. G. (1987). DNA-DNA hybridization evidence of the rapid rate of muroid rodent DNA evolution. Mol. Biol. Evol. 4: 242–253.Google Scholar
  11. Cooper, R. A., and Millener, P. R. (1993). The New Zealand biota: historical background and research. Trends Ecol. Evol. 8: 429–433.Google Scholar
  12. Daniel, M. J. (1975). First record of an Australian fruit bat (Megachiroptera: Pteropodidae) reaching New Zealand. N.Z. J. Zool. 2: 227–231.Google Scholar
  13. Daniel, M. J. (1979). The New Zealand short-tailed bat, Mystacina tuberculata: A review of present knowledge. N.Z. J. Zool. 6: 357–370.Google Scholar
  14. Daniel, M. J. (1990). Order Chiroptera. In: The Handbook of New Zealand Mammals, C. M. King, ed., pp. 114–136, Oxford University Press, Auckland.Google Scholar
  15. Daniel, M. J., and Williams, G. R. (1984). A survey of the distribution, seasonal activity and roost sites of New Zealand bats. N.Z. J. Ecol. 7: 9–25.Google Scholar
  16. Dieffenbach, E. (1843). Travels in New Zealand: With Contributions to the Geography, Geology, Botany, and Natural History of that Country, J. Murray, London. [Appendix on the mammals of New Zealand by J. E. Gray.]Google Scholar
  17. Dobson, G. E. (1875). Conspectus of the suborders, families and genera of Chiroptera arranged according to their natural affinities. Ann. Mag. Nat. Hist. 16 (Ser. 4): 345–357.Google Scholar
  18. Ducrocq, S., Jaeger, J.-J., and Sigé, B. (1993). Un mégachiroptère dans l'Eocène supérieur de Thaïlande incidence dans la discussion phylogénique du group. N. Jahr. Geol. Paläont. Monatschefte 1993: 561–575.Google Scholar
  19. Felsenstein, J. (1993). PHYLIP, Phylogenetic Inference Package, Program and Documentation, Version 3.5c, University of Washington, Seattle.Google Scholar
  20. Fenton, M. B. (1992). Bats, Facts on File, New York.Google Scholar
  21. Gall, L. F., and Tiffney, B. H. (1983). A fossil noctuid moth egg from the late Cretaceous of Eastern North America. Science 219: 507–509.Google Scholar
  22. Gray, J. E. (1821). On the natural arrangement of vertebrose animals. London Med. Reposit. 15(1): 296–310.Google Scholar
  23. Gray, J. E. (1843). List of the Specimens of Mammalia in the Collection of the British Museum, George Woodfall and Son, London.Google Scholar
  24. Hand, S. J. (1984). Bat beginnings and biogeography: A southern perspective. In: Vertebrate Zoogeography and Evolution in Australasia, M. Archer and G. Clayton, eds., pp. 853–904, Hesperian Press, Perth.Google Scholar
  25. Hand, S. J., and Kirsch, J. A. W. (1998). A southern origin for the Hipposideridae (Microchiroptera)? Evidence from the Australian fossil record. In: Bats: Phylogeny, Morphology, Echolocation, and Conservation Biology, T. H. Kunz and P. A. Racey, eds., Smithsonian Institution Press, Washington, DC (in press).Google Scholar
  26. Hand, S. J., Novacek, M., Godthelp, H., and Archer, M. (1994). First Eocene bat from Australia. J. Vert. Paleontol. 14: 375–381.Google Scholar
  27. Hand, S. J., Murray, P., Megirian, D., Archer, M., and Godthelp, H. (1998). Mystacinid bats from the Australian Tertiary. J. Paleontol. (in press).Google Scholar
  28. Hershkovitz, P. (1972). The recent mammals of the neotropical region: A zoogeographic and ecological review. In: Evolution, Mammals, and Southern Continents, A. Keast, F. C. Erk, and B. Glass, eds., pp. 311–431, State University of New York Press, Albany.Google Scholar
  29. Hill, J. E., and Daniel, M. J. (1985). Systematics of the New Zealand short-tailed bat Mystacina Gray, 1843 (Chiroptera, Mystacinidae). Bull. Br. Mus. (Nat. Hist.) Zool. Ser. 48: 279–300.Google Scholar
  30. Hill, J. E., and Smith, J. D. (1980). Bats: A Natural History, University of Texas Press, Austin.Google Scholar
  31. Hollar, L. J., and Springer, M. S. (1997). Old World fruitbat phylogeny: Evidence for convergent evolution and an endemic African clade. Proc. Natl. Acad. Sci. USA 94: 5716–5721.Google Scholar
  32. Hutcheon, J. M., Kirsch, J. A. W., and Pettigrew, J. D. (1998). Base-compositional biases and the bat problem. III. The question of microchiropteran monophyly. Phil. Trans. Roy. Soc. B 353: 607–617.Google Scholar
  33. International Commission on Zoological Nomenclature (1985). International Code of Zoological Nomenclature, 3rd ed., W. D. L. Ride, C. W. Sabrosky, G. Bernardi, and K. V. Melville, eds., University of California Press, Berkeley.Google Scholar
  34. Jepsen, G. L. (1970). Bat origins and evolution. In: Biology of Bats, W. A. Wimsatt, ed., pp. 1–64, Academic Press, London.Google Scholar
  35. Jukes, T. H., and Cantor, C. R. (1969). Evolution of protein molecules. In: Mammalian Protein Metabolism, H. N. Munro, ed., pp. 21–123, Academic Press, New York.Google Scholar
  36. Kirsch, J. A. W., and Palma, R. E. (1995). DNA/DNA hybridization studies of carnivorous marsupials. V. A further estimate of relationships among opossums (Marsupialia: Didelphidae). Mammalia 59: 403–425.Google Scholar
  37. Kirsch, J. A. W., and Pettigrew, J. D. (1998). Base-compositional biases and the bat problem. II. DNA-hybridization trees based on tracers enriched for AT-or GC-content. Phil. Trans. Roy. Soc. B 353: 381–388.Google Scholar
  38. Kirsch, J. A. W., Springer, M. S., Krajewski, C., Archer, M., Aplin, K., and Dickerman, A. W. (1990). DNA/DNA hybridization studies of carnivorous marsupials. I. The intergeneric relationships of bandicoots (Marsupialia: Perameloidea). J. Mol. Evol. 30: 434–448.Google Scholar
  39. Kirsch, J. A. W., Flannery, T. F., Springer, M. S., and Lapointe, F.-J. (1995a). Phylogeny of the Pteropodidae (Mammalia: Chiroptera) based on DNA hybridisation, with evidence for bat monophyly. Aust. J. Zool. 43: 395–428.Google Scholar
  40. Kirsch, J. A. W., Lapointe, F.-J., and Foeste, A. (1995b). Resolution of portions of the kangaroo phylogeny (Marsupialia: Macropodidae) using DNA hybridization. Biol. J. Linn. Soc. 55: 309–328.Google Scholar
  41. Kirsch, J. A. W., Lapointe, F.-J., and Springer, M. S. (1997). DNA-hybridisation studies of marsupials and their implications for metatherian classification. Aust. J. Zool. 45: 211–280.Google Scholar
  42. Koopman, K. F. (1984). Bats. In: Orders and Families of Recent Mammals of the World, S. Anderson and J. K. Jones, eds., pp. 145–186, John Wiley & Sons, New York.Google Scholar
  43. Koopman, K. F. (1994). Chiroptera: Systematics. Handbook of Zoology, VIII, 60, Mammalia, Walter de Gruyter, Berlin.Google Scholar
  44. Krajewski, C., and Dickerman, A. W. (1990). Bootstrap analysis of phylogenetic trees derived from DNA hybridization distances. Syst. Zool. 39: 383–390.Google Scholar
  45. Landry, P.-A., Lapointe, F.-J., and Kirsch, J. A. W. (1996). Estimating phylogenies from lacunose distance matrices: Additive is superior to ultrametric estimation. Mol. Biol. Evol. 13: 818–823.Google Scholar
  46. Lapointe, F.-J., Kirsch, J. A. W., and Bleiweiss, R. (1994). Jackknifing of weighted trees: Validation of phylogenies reconstructed from distance matrices. Mol. Phylogenet. Evol. 3: 256–267.Google Scholar
  47. Maddison, W. P., and Maddison, D. R. (1993). MacClade Analysis of Phylogeny and Character Evolution, Version 3, Sinauer Associates, Sunderland, MA.Google Scholar
  48. McKenna, M. C., and Bell, S. K. (1997). Classification of Mammals Above the Species Level, Columbia University Press, New York.Google Scholar
  49. Meschinelli, L. (1903). Un nuovo chiroptero fossile (Archaeopteropus transiens Meschen.) delle liquiti di Monteviale. Atti. Istituto Veneto di Scienze, Lettere, ed Arti (Venezia). Classe di Scienze Fisiche, Matematiche, e Naturali 62: 1329–1344.Google Scholar
  50. Miller, G. S. (1907). The families and genera of bats. Bull. U.S. Natl. Mus. 57:i–xvii, 1–282.Google Scholar
  51. Molloy, J. (1995). Bat (peka peka) recovery plan (Mystacina, Chalinolobus). Threatened Species Recovery Plan Series 15, Publ. Dept. Conserv., Wellington, New Zealand.Google Scholar
  52. Molloy, J., and Davis, A. (1994). Setting Priorities for the Conservation of New Zealand's Threatened Plants and Animals, 2nd ed., Publ. Dept. Conserv., Wellington, New Zealand.Google Scholar
  53. Novacek, M. J. (1991). Aspects of morphology of the cochlea in microchiropteran bats: An investigation of character transformation. Bull. Am. Mus. Nat. Hist. 206: 84–100.Google Scholar
  54. Page, R. D. M. (1996). TREEVIEW: An application to display phylogenetic trees on personal computers. Comp. Appl. Biosci. 12: 357–358.Google Scholar
  55. Peters, W. (1865). Abbildungen zu einer Monographie der Chiropteren vor und gab einer Übersicht der von ihm befolgten systematischen Ordnung der hieher gehörigen Gattungen. Monatsberg. K. Preuss. Akad. Wissensch. Berlin 1865: 256–258.Google Scholar
  56. Pettigrew, J. D., and Kirsch, J. A. W. (1995). Flying primates revisited: DNA hybridization with fractionated, GC-enriched DNA. S. Afr. J. Sci. 91: 477–482.Google Scholar
  57. Pettigrew, J. D., Jamieson, B. G. M., Robson, S. K., Hall, L. S., McNally, K. I., and Cooper, H. M. (1989). Phylogenetic relations between microbats, megabats and primates (Mammalia: Chiroptera and Primates). Phil. Trans. Roy. Soc. B 235: 489–559.Google Scholar
  58. Pierson, E. D. (1986). Molecular Systematics of the Microchiroptera: Higher Taxon Relationships and Biogeography, Unpublished Ph.D. thesis, University of California, Berkeley.Google Scholar
  59. Pierson, E. D., Sarich, V. M., Lowenstein, J. M., Daniel, M. J., and Rainey, W. E. (1986). A molecular link between the bats of New Zealand and South America. Nature (London) 323: 60–63.Google Scholar
  60. Porter, C. A., Goodman, M., and Stanhope, M. J. (1996). Evidence on mammalian phylogeny from sequences of exon 28 of the von Willebrand factor gene. Mol. Phylogenet. Evol. 5: 89–101.Google Scholar
  61. Roeder, K. D., and Treat, A. E. (1962). The detection and evasion of bats by moths. Smithson. Rep. 1961: 455–464.Google Scholar
  62. Sarich, V. M., and Cronin, J. E. (1976). Molecular systematics of the primates. In: Molecular Anthropology, Genes, and Proteins in the Evolutionary Ascent of the Primates, M. Goodman and R. E. Tashian, eds., pp. 141–170, Plenum Press, New York.Google Scholar
  63. Sheldon, F. H., and Bledsoe, A. H. (1989). Indexes to the reassociation and stability of solution DNA hybrids. J. Mol. Evol. 29: 328–343.Google Scholar
  64. Sibley, C. G., and Ahlquist, J. E. (1981). The phylogeny and relationships of the ratite birds as indicated by DNA-DNA hybridization. In: Evolution Today, G. G. E. Scudder and J. L. Reveal, eds., pp. 301–335, Carnegie-Mellon University, Pittsburgh.Google Scholar
  65. Sibley, C. G., and Ahlquist, J. E. (1990). Phylogeny and Classification of Birds: A Study in Molecular Evolution, Yale University Press, New Haven, CT.Google Scholar
  66. Sigé, B. (1977). Les insectivores et chiroptères du Paléogène moyen d'Europe dans l'histoire des faunes de mammifères sur ce continent. Jurij A. Orlov Memorial. J. Paleontol. Soc. India 20: 178–190.Google Scholar
  67. Sigé, B. (1991). Rhinolophoidea et Vespertilionoidea (Chiroptera) du Chambi (Eocène inférieur de Tunisie) aspects biostratigraphique, biogéographique et paléoécologique de l'origine des chiroptères modernes. N. Jahr. Geol. Paläont. Abhandlungen 182: 355–376.Google Scholar
  68. Sigé, B. (1993). Toward a phylogeny of bats. Poster, Fourth Congress of the European Society for Evolutionary Biology, Montpellier, France.Google Scholar
  69. Simmons, N. B. (1998). A reappraisal of interfamilial relationships of bats. In: Bats: Phylogeny, Morphology, Echolocation, and Conservation Biology, T. H. Kunz and P. A. Racey, eds., Smithsonian Institution Press, Washington, DC (in press).Google Scholar
  70. Simmons, N. B., and Geisler, J. H. (1998). Phylogenetic relationships of Icaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx to extant bat lineages, with comments on the evolution of echolocation and foraging strategies in Microchiroptera. Bull. Am. Mus. Nat. Hist. 235: 1–182.Google Scholar
  71. Simpson, G. G. (1945). The principles of classification and a classification of mammals. Bull. Am. Mus. Nat. Hist. 85:vi–xvi, 1–350.Google Scholar
  72. Smith, A. B. (1994). Rooting molecular trees: Problems and strategies. Biol. J. Linn. Soc. 51: 279–292.Google Scholar
  73. Smith, J. D. (1976). Chiropteran evolution. In: Biology of Bats of the New World Family Phyllostomatidae, Part I, R. J. Baker, J. K. Jones, and D. C. Carter, eds., pp. 49–69, Spec. Publ. Mus., Texas Tech Univ. No. 10, Texas Tech University, Lubbock.Google Scholar
  74. Springer, M. S. (1997). Molecular clocks and the timing of the placental and marsupial radiations in relation to the Cretaceous-Tertiary boundary. J. Mammal. Evol. 4: 285–302.Google Scholar
  75. Springer, M. S., and Kirsch, J. A. W. (1991). DNA hybridization, the compression effect, and the radiation of diprotodontian marsupials. Syst. Zool. 40: 131–151.Google Scholar
  76. Springer, M. S., Davidson, E. H., and Britten, R. J. (1992). Calculation of sequence divergence from the thermal stability of DNA heteroduplexes. J. Mol. Evol. 34: 379–382.Google Scholar
  77. Sullivan, J., and Swofford, D. L. (1997). Are guinea pigs rodents? The importance of adequate models in molecular phylogenetics. J. Mammal. Evol. 4: 77–86.Google Scholar
  78. Swofford, D. L. (1993). PAUP: Phylogenetic Analysis Using Parsimony, Version 3.1, Illinois Natural History Survey, Champaign.Google Scholar
  79. Thomas, O. (1905). On some Australasian mammals. Ann. Mag. Nat. Hist. (7), 16: 422–428.Google Scholar
  80. Tomes, R. F. (1857). On two species of bats inhabiting New Zealand. Proc. Zool. Soc. Lond. 1857: 233–244.Google Scholar
  81. Tomes, R. F. (1863). On a new genus and species of leaf-nosed bats in the museum at Fort Pitt. Proc. Zool. Soc. Lond. 1863: 81–84.Google Scholar
  82. Winge, H. (1892). Jordfundne og nulevende Flagermus (Chiroptera) fra Lagoa Santa, Minas Geraes, Brasilien. Museo Lundii 2(1): 1–65.Google Scholar
  83. Woodburne, M. O., and Case, J. A. (1996). Dispersal, vicariance, and the Late Cretaceous to Early Tertiary land mammal biogeography from South America to Australia. J. Mammal. Evol. 3: 121–161.Google Scholar
  84. Van Valen, L. (1979). The evolution of bats. Evol. Theory 4: 103–121.Google Scholar
  85. Veevers, J. J. (1991). Phanerozoic Australia in the changing configuration of proto-Pangea through Gondwanaland and Pangea to the present dispersed continents. Aust. Syst. Bot. 4: 1–11.Google Scholar

Copyright information

© Plenum Publishing Corporation 1998

Authors and Affiliations

  • John A. W. Kirsch
  • James M. Hutcheon
  • Deanna G. P. Byrnes
  • Brian D. Lloyd

There are no affiliations available

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