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, 130:169 | Cite as

Genetic divergence and phylogeography in the genus Nyctalus (Mammalia, Chiroptera): implications for population history of the insular bat Nyctalus azoreum

  • P. Salgueiro
  • M. Ruedi
  • M. M. Coelho
  • J. M. Palmeirim
Original Paper

Abstract

We used three mitochondrial DNA fragments with different substitution rates (ND1, Cyt b and the CR) to infer phylogenetic relationships among six species of the genus Nyctalus, and compare levels of genetic divergence between the insular, vulnerable Nyctalus azoreum and its continental counterpart to assess the origins of the Azorean bat. The larger species found throughout the Palaearctic region (N. lasiopterus, N. aviator and N. noctula) share a unique chromosome formula (2n = 42) and form a monophyletic clade in our reconstructions. Nyctalus plancyi (= velutinus), a Chinese taxon with 2n = 36 chromosomes, is sometimes included in N. noctula, but is genetically very divergent from the latter and deserves full species status. All Cyt b and CR haplotypes of N. azoreum are closely related and only found in the Azores archipelago, but when compared to continental sequences of N. leisleri, levels of mtDNA divergence are unusually low for mammalian species. This contrasts with the high level of differentiation that N. azoreum has attained in its morphology, ecology, and echolocation calls, suggesting a recent split followed by fast evolutionary change. The molecular data suggest that N. azoreum originated from a European population of N. leisleri, and that the colonisation of the Azores occurred at the end of the Pleistocene. The Madeiran populations of N. leisleri also appear to have a European origin, whereas those of the Canary Islands probably came from North Africa. In spite of its recent origin and low genetic divergence, the Azorean bat is well differentiated and consequently represents a unique evolutionary unit with great conservation value.

Keywords

Azores Bat Colonisation Mitochondrial DNA Phylogeography Nyctalus azoreum Nyctalus leisleri 

Notes

Acknowledgments

We are indebted to the people who helped in the field, including: Ana Cerveira, Filipe Moniz, Mafalda Frade, Filipe Canário, Mário Silva, Helder Fraga, Fernando Pereira, Margarida Leonardo, Sofia Lourenço and Sophie Vancoille. We are grateful to Maria José Pitta and André Silva from the Direcção Regional de Ambiente dos Açores for processing the permit to handle bats. We also would like to thank the samples donated by A. Rainho (I.C.N.), J. Juste, C. Ibañez, D. Trujillo (I.B.D.), and Petr Benda (N.M.P., grant 206/05/2334 from the Grant Agency of the Czech Republic). José Farni and Benoît Stadelmann provided help during the sequencing at Geneva. Anabel Perdices gave advice on the phylogenetic analysis. We would also like to thank the Muséum d’Histoire Naturelle de Genève and anonymous reviewers. This research was funded by Fundação para a Ciência e Tecnologia (project POCTI: BSE/33963/99–00), and a PhD grant to P.S. (SFRH/BD/1201/2000), co-financed by the European Regional Development Fund.

References

  1. Avise JC, Walker D (1999) Species realities and numbers in sexual vertebrates: perspectives from an asexually transmitted genome. Proc Natl Acad Sci USA 96:992–995PubMedCrossRefGoogle Scholar
  2. Bandelt H, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16: 37–48PubMedGoogle Scholar
  3. Barratt EM, Deaville R, Burland TM, Bruford MW, Jones G, Racey PA, Wayne RK (1997) DNA answers the call of pipistrelle bat species. Nature 387:138–139PubMedCrossRefGoogle Scholar
  4. Beheregaray LB, Gibbs JP, Havill N, Fritts TH, Powell JR, Caccone A (2004) Giant tortoises are not so slow: rapid diversification and biogeographic consensus in the Galapagos. Proc Natl Acad Sci USA 101:6514–6519PubMedCrossRefGoogle Scholar
  5. Borges PAV, Brown VK (1999) Effect of island geological age on the arthropod species richness of Azorean pastures. Biol J Linn Soc 66:373–410CrossRefGoogle Scholar
  6. Bradley RD, Baker RJ (2001) A test of the genetic species concept: cytochrome b sequences and mammals. J Mammal 82:960–973CrossRefGoogle Scholar
  7. Bunce M, Szulkin M, Lerner H, Barnes I, Shapiro B, Cooper A, Holdaway R (2005) Ancient DNA provides new insights into the evolutionary history of New Zealand’s extinct giant eagle. PLoS Biol 3:e9PubMedCrossRefGoogle Scholar
  8. Castella V, Ruedi M, Excoffier L (2001) Contrasted patterns of mitochondrial and nuclear structure among nursery colonies of the bat Myotis myotis. J Evol Biol 14:708–720CrossRefGoogle Scholar
  9. Chiroptera Specialist Group (2000). Nyctalus azoreum. In: IUCN 2006. 2006 IUCN Red List of Threatened Species. <http://www.iucnredlist.org>. Downloaded on 01 June 2006
  10. Corbet GB (1978) The mammals of the Palaearctic Region: a taxonomic review. Cornell University Press, London, 314 ppGoogle Scholar
  11. Corbet GB, Hill JE (1992) The mammals of the Indomalayan region: a systematic review. Nat. Hist. Mus. Publ. Oxford University Press, Oxford, 488 ppGoogle Scholar
  12. Excoffier L, Smouse PE (1994) Using allele frequencies and geographic subdivision to reconstruct gene trees within a species: molecular variance parsimony. Genetics 136:343–359PubMedGoogle Scholar
  13. Fumagalli L, Taberlet P, Favre L, Hausser J (1996) Origin and evolution of homologous repeated sequences in the mitochondrial DNA control region of shrews. Mol Biol Evol 13:31–46PubMedGoogle Scholar
  14. Glor RE, Kolbe JJ, Powell R, Larson A, Losos JB (2003) Phylogenetic analysis of ecological and morphological diversification in hispaniolan trunk-ground Anoles (Anolis cybotes group). Evolution 57:2383–2397PubMedGoogle Scholar
  15. Grant PR, Grant BR (1997) Genetics and the origin of bird species. Proc Natl Acad Sci USA 94:7768–7775PubMedCrossRefGoogle Scholar
  16. Hasegawa M, Kishino H, Yano T (1985) Dating of the human–ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 21:160–174CrossRefGoogle Scholar
  17. Hounsome MV (1993) Biometrics and origins of some Atlantic island birds. Bol Mus Municipal Funchal 2:107–129Google Scholar
  18. Imaizumi Y (1970) The handbook of Japanese land mammals. Shin-Schicho-Sha, TokyoGoogle Scholar
  19. Juste J, Ibañez C, Muñoz J, Trujillo D, Benda P, Karatas A, Ruedi M (2004) Mitochondrial phylogeography of the long-eared bats (Plecotus) in the Mediterranean Palaearctic and Atlantic Islands. Mol Phylogenet Evol 31:1114–1126PubMedCrossRefGoogle Scholar
  20. Juste J, Ibañez C, Trujillo D, Muñoz J, Ruedi M (2003) Phylogeography of barbastelle bats in the western Mediterranean and the Canary Islands. Acta Chiropt 5:165–175Google Scholar
  21. Kawai K, Nikaido M, Harada M, Matsumura S, Lin LK, Wu Y, Hasegawa M, Okada N (2002) Intra- and interfamily relationships of Vespertilionidae inferred by various molecular markers including SINE insertion data. J Mol Evol 55:284–301PubMedCrossRefGoogle Scholar
  22. Kiefer A, Veith M (2002) A new species of long-eared bat from Europe (Chiroptera: Vespertiliondae). Myotis 39:5–16Google Scholar
  23. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:11–120CrossRefGoogle Scholar
  24. Koopman KF (1994) Chiroptera: systematics. In: Niethammer J, Schliemann H, Starck. D (eds) Handbuch der Zoologie. de Gruyter, Berlin, pp 100–109Google Scholar
  25. Kvist L, Broggi J, Illera JC Koivula K (2005) Colonisation and diversification of the blue tits (Parus caeruleus teneriffae-group) in the Canary Islands. Mol Phylogenet Evol 34:501–511PubMedCrossRefGoogle Scholar
  26. Le Grand G (1984) Réflexions sur le peuplement de la Macaronésie. Arquipélago 5:87–101Google Scholar
  27. Lin L-K, Motokawa M, Harada M (2002) Karyology of ten vespertilionid bats (Chiroptera: Vespertilionidae) from Taiwan. Zool Stud 41:347–354Google Scholar
  28. Macdonald DW, Barrett P (1993) Collins field guide to mammals of Britain and Europe. Collins, London, pp 312Google Scholar
  29. Maddison WP, Maddison DR (1992) MacClade v.3. Analysis of phylogeny and character evolution. Sinauer Associates, SunderlandGoogle Scholar
  30. Maeda K (1983) Classificatory study of the Japanese Large Noctule, N. lasiopterus aviator (Thomas, 1911). Zool Mag 92:21–36Google Scholar
  31. Maharadatunkamsi SH, Kitchener DJ, Schmitt LH (2003) Relationships between morphology, genetics and geography in the cave fruit bat Eonycteris spelaea (Dobson, 1871) from Indonesia. Biol J Linn Soc 79:511–522CrossRefGoogle Scholar
  32. Mayer F, von Helversen O. (2001) Cryptic diversity in European bats. Proc R Soc Lond B Biol Sci 268:1825–1832CrossRefGoogle Scholar
  33. Mayr E (1942) Systematics and the origin of species. Columbia University Press, New YorkGoogle Scholar
  34. Mayr E, Ashlock PD (1991) Principles of systematic zoology. McGraw-Hill, New York, pp 475Google Scholar
  35. Miller GS (1912) Catalogue of the mammals of Western Europe (Europe exclusive of Russia) in the collection of the British Museum. Trustees of the British Museum (Natural History), LondonGoogle Scholar
  36. Miller SA, Dykes DD, Polesky HF (1988) A simple salting procedure for extracting DNA from human nucleated cells. Nucl Acids Res 16:215Google Scholar
  37. Moore NW (1975) The diurnal flight of the Azorean bat (Nyctalus azoreum) and the avifauna of the Azores. J Zool 177:483–466CrossRefGoogle Scholar
  38. Nikaido M, Kawai K, Cao Y, Harada M, Tomita S, Okada N, Hasegawa M (2001) Maximum likelihood analysis of the complete mitochondrial genomes of eutherians and a reevaluation of the phylogeny of bats and insectivores. J Mol Evol 53:508–516PubMedCrossRefGoogle Scholar
  39. Palmeirim JM (1991) A morphometric assessment of the systematic position of the Nyctalus from Azores and Madeira (Mammalia: Chiroptera). Mammalia 55:381–388CrossRefGoogle Scholar
  40. Pamilo P, Nei M (1988) Relationships between gene trees and species trees. Mol Biol Evol 5:568–583PubMedGoogle Scholar
  41. Pestano J, Brown RP, Suárez NM, Fajardo S (2003) Phylogeography of pipistrellle-like bats within the Canary Islands, based on mtDNA sequences. Mol Phylogenet Evol 26:56–63PubMedCrossRefGoogle Scholar
  42. Petit E, Excoffier L, Mayer F (1999) No evidence of bottleneck in the postglacial recolonisation of Europe by the noctule bat (Nyctalus noctula). Evolution 53:1247–1258CrossRefGoogle Scholar
  43. Polly PD (2001) On morphological clocks and paleophylogeography: towards a timescale for Sorex hybrid zones. Genetica 112–113:339–357Google Scholar
  44. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  45. Posada D, Crandall KA (2001) Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 16:37–45PubMedCrossRefGoogle Scholar
  46. Queiroz AI, Alves PC, Barroso I, Beja P, Fernandes M, Freitas L, Mathias ML, Mira A, Palmeirim JM, Prieto R, Rainho A, Rodrigues L, Santos-Reis M, Sequeira M (2006) Nyctalus azoreum Morcego dos Açores. In: Cabral MJ, Almeida J, Almeida PR, Dellinger T, Ferrand de Almeida N, Oliveira ME, Palmeirim JM, Queiroz AI, Rogado L, Santos-Reis M (eds) Livro Vermelho dos Vertebrados de Portugal, 2nd edn. Instituto da Conservação da Natureza/Assírio and Alvim, Lisboa, pp 463–464Google Scholar
  47. Rainho A, Marques JT, Palmeirim JM (2002) Os morcegos dos arquipélagos dos Açores e da Madeira: um contributo para a sua conservação. Instituto da Conservação da Natureza, LisboaGoogle Scholar
  48. Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:1095–1103PubMedGoogle Scholar
  49. Rodriguez F, Oliver J, Marin A, Medina J (1990) The general stochastic model of nucleotide substitutions. J Theor Biol 142:485–501PubMedGoogle Scholar
  50. Röhl A (2004) Network: a program package for calculating phylogenetic networks, version 4.1.0.9. Fluxus Technology Ltd., HamburgGoogle Scholar
  51. Ruedi M, Mayer F (2001) Molecular systematics of bats of the genus Myotis (Vespertilionidae) suggests deterministic ecomorphological convergences. Mol Phylogenet Evol 21:436–448PubMedCrossRefGoogle Scholar
  52. Ruedi M, McCracken GF (2006) Genetics and evolution: phylogeographic analysis. In: Kunz TH, Parsons S (eds) Ecological and behavioral methods for the study of bats, 2nd edn. Johns Hopkins University Press, Boston (in press)Google Scholar
  53. Salgueiro P, Coelho MM, Palmeirim JM, Ruedi M (2004) Mitochondrial DNA variation and population structure of the island endemic Azorean bat (Nyctalus azoreum). Mol Ecol 13:3357–3366PubMedCrossRefGoogle Scholar
  54. Schmitt LH, Kitchener DJ, How RA (1995) A genetic prespective of mammalian variation and evolution in the indonesian archipelago: biogeographic correlates in the fruit bat genus Cynopterus. Evolution 49:399–412CrossRefGoogle Scholar
  55. Simmons NB (2005) Order Chiroptera. In: Wilson DE, Reeder DM (eds) Mammal species of the world. A taxonomic and geographic reference, 3rd edn. Smithsonian Institution Press, WashingtonGoogle Scholar
  56. Skiba R (1996) Nachweis einer Zwergfledermaus, Pipistrellus pipistrellus (Schreiber 1774), auf der Azorinsel Flores (Portugal). Myotis 34:81–84Google Scholar
  57. Skiba R. (2003) Europäische Fledermäuse. Kennzeichen, Echoortung und Detektoranwendung. Westarp Wissenschaften, Hohenwarsleben, Germany, pp 212Google Scholar
  58. Smith M, Patton J (1993) The diversification of South American murid rodents. Evidence from mitochondrial DNA sequence data for the akodontine tribe. Biol J Linn Soc 50:149–177CrossRefGoogle Scholar
  59. Soulé ME (1989) Conservation biology in the twenty-first century: summary and outlook. In: Western D, Pearl M (eds) Conservation for the twenty-first century. Oxford University Press, New York, pp 297–303Google Scholar
  60. Speakman JR (1995) Chiropteran nocturnality. In: Racey PA, Swift SM (eds) Ecology, evolution and behaviour of bats. Symposium 67 of the Zoological Society of London, Oxford University, Oxford, pp 187–201Google Scholar
  61. Speakman JR, Webb PI (1993) Taxonomy, status and distribution of the Azorean bat (Nyctalus azoreum). J Zool 231:27–38CrossRefGoogle Scholar
  62. Spitzenberger F, Haring E, Tvrtkovic N (2002) Plecotus microdontius (Mammalia, Vespertilionidae), a new bat species from Austria. Natura Croatica 11:1–18Google Scholar
  63. Swofford DL (1998) PAUP*: phylogenetic analysis using parsimony and other methods, version 4.0. Sinauer Associates, SunderlandGoogle Scholar
  64. Tate GH (1942) Results of the Archbold expeditions. No. 47: review of the Vespertilionine bats. Bull Am Mus Nat Hist 80:221–297Google Scholar
  65. Thomas O (1901) On some new African bats. Ann Mag Nat Hist 7:34Google Scholar
  66. Tregenza T, Bridle JR (1997) The diversity of speciation. Trends Ecol Evol 12:382–383CrossRefGoogle Scholar
  67. Tregenza T (2002) Divergence and reproductive isolation in the early stages of speciation. Genetica 116:291–300PubMedCrossRefGoogle Scholar
  68. Volleth M (1992) Comparative analysis of the banded karyotypes of the European Nyctalus species (Vespertilionidae; Chiroptera). Charles University Press, PragueGoogle Scholar
  69. Wiens JJ (2004) What is speciation and how should we study it? Am Nat 163:914–923PubMedCrossRefGoogle Scholar
  70. Zhang W (1990) A study of karyotype and C-banding pattern of Nyctalus velutinus. J Anhui Normal Univ 4:58–63Google Scholar
  71. Zwartjes PW (2003) Genetic variability in migratory and endemic island songbirds (genus Vireo): a comparative assessment using molecular and morphological traits. Conserv Genet 4:749–758CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • P. Salgueiro
    • 1
  • M. Ruedi
    • 2
  • M. M. Coelho
    • 1
  • J. M. Palmeirim
    • 1
  1. 1.Centro de Biologia Ambiental/Departamento de Biologia AnimalFaculdade de Ciências da Universidade de LisboaLisboaPortugal
  2. 2.Muséum d’Histoire Naturelle de GenèveGeneva 6Switzerland

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