Translator Disclaimer
1 December 2004 Phylogeny of African Myotis Bats (Chiroptera, Vespertilionidae) Inferred from Cytochrome b Sequences
Benoît Stadelmann, David S. Jacobs, Corrie Schoeman, Manuel Ruedi
Author Affiliations +

The genus Myotis is comprised of about 100 species that are unequally distributed between the Northern (81% of the species) and the Southern hemisphere (19% of the species). Only eight species of Myotis occur in the Ethiopian region, but this is the only biogeographic region with representatives of all four classical subgenera, suggesting a diverse assemblage of morphotypes. We used sequences of a mitochondrial DNA gene (cyt b) to investigate the evolution and the phylogenetic position of seven of the eight Ethiopian species, and compared them to a broad sampling of Myotis from the World and of other vespertilionids. Phylogenetic reconstruction was based on 91 complete sequences representing 79 species of bats. The two endemic southern African species of the subgenus Cistugo were not placed within the genus Myotis, but were basal to the vespertilionid radiation, as suggested by earlier work based on karyology. The remaining Ethiopian species formed a strong monophyletic clade within Myotis, further stressing the importance of biogeography as a good predictor of phylogenetic relationships. This Ethiopian clade includes one Western Palaearctic and one Oriental species, both of which probably secondarily colonized these areas from the Ethiopian region. Molecular dating based on Bayesian inferences suggest that these faunal exchanges occurred at the end of the Miocene, while the split of the Ethiopian clade from the other Old World Myotis dates back to the middle Miocene, quite early in the Myotis radiation. Thus, the relative paucity of species in sub-Saharan Africa cannot be attributed to a late entry into this continent. Instead, these molecular results suggest that other evolutionary processes are responsible for the poor species diversity of Myotis found in Africa today.



P. T. Agirre-Mendi , J. L. García-Mudarra , J. Juste , and C. Ibáñez . 2004. Presence of Myotis alcathoe Helversen & Heller, 2001 (Chiroptera: Vespertilionidae) in the Iberian Peninsula. Acta Chiropterologica, 6: 49–57. Google Scholar


B. R. Appleton , J. A. Mckenzie , and L. Christidis . 2004. Molecular systematics and biogeography of the bent-wing bat complex Miniopterus schreibersii (Kuhl, 1817) (Chiroptera: Vespertilionidae). Molecular Phylogenetics and Evolution, 31: 431–439. Google Scholar


P. Benda , M. Ruedi , and M. Uhrin . 2003. First record of Myotis alcathoe (Chiroptera: Vespertilionidae) in Slovakia. Folia Zoologica, 52: 359–365. Google Scholar


J. W. Bickham , K. Mcbee , and D. A. Schlitter . 1986. Chromosomal variation among seven species of Myotis (Chiroptera: Vespertilionidea). Journal of Mammalogy, 67: 746–750. Google Scholar


J. W. Bickham , J. C. Patton , D. A. Schlitter , I. L. Rautenbach , and R. L. Honeycutt . 2004. Molecular phylogenetics, karyotypic diversity, and partition of the genus Myotis (Chiroptera: Vespertilionidae). Molecular Phylogenetics and Evolution, 33: 333–338. Google Scholar


P. Chomczynski , and N. Sacchi . 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry, 162: 156–159. Google Scholar


C. J. Douady , and E. J. P. Douzery . 2003. Molecular estimation of eulipotyphlan divergence times and the evolution of ‘Insectivora’. Molecular Phylogenetics and Evolution, 28: 285–296. Google Scholar


J. Fahr and N. M. Ebigbo . 2003. A conservation assessment of the bats of the Simandou Range, Guinea, with the first record of Myotis welwitschii (Gray, 1866) from West Africa. Acta Chiropterologica, 5: 125–141. Google Scholar


J. S. Farris 1989. The retention index and the rescaled consistency index. Cladistics, 5: 417–419. Google Scholar


J. Felsenstein 1984. Distance methods for inferring phylogenies — a justification. Evolution, 38: 16–24. Google Scholar


J. Felsenstein 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution, 39: 783–791. Google Scholar


J. Felsenstein 1993. PHYLIP (Phylogeny Inference Package), Version 3.6. University of Washington, Seattle, WA. Google Scholar


M. B. Fenton , and W. Bogdanowicz . 2002. Relationships between external morphology and foraging behaviour: bats in the genus Myotis. Canadian Journal of Zoology, 80: 1004–1013. Google Scholar


B. M. Flower , and J. P. Kennett . 1994. The middle Miocene climatic transition: East Antartic ice sheet development, deep ocean circulation and global carbon cycling. Palaeogeography, Palaeoclimatology, Palaeoecology, 108: 537–555. Google Scholar


J. S. Findley 1972. Phenetic relationships among bats of the genus Myotis. Systematic Zoology, 21 : 31–52. Google Scholar


O. Gascuel 1997. BIONJ: An improved version of the NJ algorithm based on a simple model of sequence data. Molecular Biology and Evolution, 14: 685–695. Google Scholar


J. Godawa Stormark 1998. Phenetic analysis of Old World Myotis (Chiroptera: Vespertilionidae) based on dental characters. Acta Theriologica, 43: 1–11. Google Scholar


S. Guindon , and O. Gascuel . 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum Likelihood. Systematic Biology, 52: 696–704. Google Scholar


T. A. Hall 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41: 95–98. Google Scholar


J. E. Hill , and P. Morris . 1971. Bats from Ethiopia collected by the Great Abbai Expedition 1968. Bulletin of the British Museum, Natural History (Zoology), 21: 27–49. Google Scholar


J. E. Hill , D. L. Harrison , and T. S. Jones . 1988. New records of bats (Microchiroptera) from Nigeria. Mammalia, 52: 590–592. Google Scholar


D. M. Hillis , and J. J. Bull . 1993. An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology, 42: 182–192. Google Scholar


S. R. Hoofer, and R. A. Van Den Bussche . 2003. Molecular phylogenetics of the Chiropteran family Vespertilionidae. Acta Chiropterologica, 5 (supplement): 1–63. Google Scholar


I. Horáček 2001. On the early history of vespertilionid bats in Europe: the Lower Miocene record from the Bohemian Massif. Lynx (N.S.), 32: 123–154. Google Scholar


I. Horáček, and V. Hanák . 1984. Comments on the systematics and phylogeny of Myotis nattereri (Kuhl, 1818). Myotis, 21–22: 20–29. Google Scholar


V. Hanák Horáček I. , and J. Gaisler . 2000. Bats of the Palaearctic region: a taxonomic and biogeographical review. Pp. 11–157, in Proceedings of the VIIIth EBRS ( B. W. Wołoszyn , ed.). Institute of Systematics and Evolution of Animals PAS, Kraków, 273 pp. Google Scholar


J. P. Huelsenbeck , and F. Ronquist . 2001. MRBAYES: Bayesian inference of phylogeny. Bioinformatics, 17: 754–755. Google Scholar


D. M. Irwin , T. D. Kocher , and A. C. Wilson . 1991. Evolution of the cytochrome b gene of mammals. Journal of Molecular Evolution, 32: 128–144. Google Scholar


K. E. Jones , A. Purvis , A. Maclarnon , O. R. P. Bininda-Emonds , and N. B. Simmons . 2002. A phylogenetic supertree of the bats (Mammalia: Chiroptera). Biological Reviews, 77: 223–259. Google Scholar


K. Kawai , M. Nikaido , M. Harada , S. Matsumura , L.-K. Lin , Y. Wu , M. Hasegawa , and N. Okada . 2002. Intra- and interfamily relationships of Vespertilionidae inferred by various molecular markers including SINE insertion data. Journal of Molecular Evolution, 55: 284–301. Google Scholar


K. Kawai , M. Nikaido , M. Harada , S. Matsumura , L.-K. Lin , Y. Wu , M. Hasegawa , and N. Okada . 2003. The status of the Japanese and East Asian bats of the genus Myotis (Vespertilionidae) based on mitochondrial sequences. Molecular Phylogenetics and Evolution, 28: 297–307. Google Scholar


H. Kishino , J. L. Thorne , and W. J. Bruno . 2001. Performance of a divergence time estimation method under a probabilistic model of rate evolution. Molecular Biology and Evolution, 18: 352–361. Google Scholar


D. Kock 2001. Identity of the African Vespertilio hesperida Temminck 1840 (Mammalia, Chiroptera, Vespertilionidae). Senckenbergiana biologica, 81: 277–283. Google Scholar


K. F. Koopman 1994. Chiroptera: Systematics. Pp. 100–109, in Handbuch der Zoologie, Vol. VII ( J. Niethammer, H. Schliemann, and D. Starck , eds.). Walter de Gruyter, Berlin, vii + 217 pp. Google Scholar


C. Lanave , G. Preparata , C. Saccone , and G. Serio . 1984. A new method for calculating evolutionary substitution rates. Journal of Molecular Evolution, 20: 86–93. Google Scholar


F. Mayer, and O. Von Helversen . 2001a. Cryptic diversity in European bats. Proceedings of the Royal Society of London, Series B, 268: 1825–1832. Google Scholar


F. Mayer, and O. Von Helversen . 2001b. Sympatric distribution of two cryptic bat species across Europe. Biological Journal of the Linnean Society, 74: 365–374. Google Scholar


I. L. Rautenbach , G. N. Bronner , and D. A. Schlitter . 1993. Karyotypic data and attendant systematic implications for the bats of southern Africa. Koedoe, 36: 87–104. Google Scholar


A. Roberts 1919. Descriptions of some new mammals. Annals of the Transvaal Museum, 6: 112–113. Google Scholar


R. Rodriguez , J. L. Olivier , A. Marin , and J. R. Medina . 1990. The general stochastic model of nucleotide substitution. Journal of Theoretical Biology, 142: 485–501. Google Scholar


M. Ruedi , and F. Mayer . 2001. Molecular systematics of bats of the genus Myotis (Vespertilionidae) suggests deterministic ecomorphological convergences. Molecular Phylogenetics and Evolution, 21: 436–448. Google Scholar


M. Ruedi , P. Jourde , P. Giosa , M. Barataud , and S. Y. Roué . 2002. DNA reveals the existence of Myotis alcathoe in France (Chiroptera: Vespertilionidae). Revue Suisse de Zoologie, 109: 643–652. Google Scholar


N. Saitou , and M. Nei . 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4: 406–425. Google Scholar


T. Sakai , Y. Kikkawa , K. Tsuchiya , M. Harada , M. Kanoe , M. Yoshiyuki , and H. Yonekawa . 2003. Molecular phylogeny of Japanese Rhinolophidae based on variations in the complete sequence of the mitochondrial cytochrome b gene. Genes and Genetic Systems, 78: 179–189. Google Scholar


I. Schunger, C. Dietz, D. Merdschanova, S. Merdschanov, K. Christov, I. Borissov, S. Staneva, and B. P. Petrov . In press. Swarming of bats at Cave Vodnite Dupki (Central Balkan National Park, Bulgaria). Acta Zoologica Bulgarica. Google Scholar


N. B. Simmons In press. Order Chiroptera. In Mammal species of the World: A taxonomic and geographic reference, third edition ( D. E. Wilson and D. M. Reeder , eds.). Smithsonian Institution Press, Washington, D.C. Google Scholar


M. F. Smith , and J. L. Patton . 1991. Variation in mitochondrial cytochrome b sequence in natural populations of South American akodontine rodents (Muridae: Sigmodontinae). Molecular Biology and Evolution, 8: 85–103. Google Scholar


B. Stadelmann , L. G. Herrera , J. Arroyocabrales , J. J. Flores-Martínez , B. P. May , and M. Ruedi . 2004. Molecular systematics of the fishing bat Myotis (Pizonyx) vivesi. Journal of Mammalogy, 85: 133–139. Google Scholar


D. L. Swofford , G. J. Olsen , P. J. Waddell , and D. M. Hillis . 1996. Phylogenetic inference, Pp. 407–514, in Molecular systematics, second edition ( D. M. Hillis, C. Moritz, and B. K. Mable , eds.). Sinauer Associates Inc., Publishers, Sunderland, Massachusets, 655 pp. Google Scholar


D. L. Swofford 2002. PAUP*. Phylogenetic analyses using parsimony (*and other methods), Version 4.0b10a for PC. Sinauer Associates Inc., Publishers, Sunderland, Massachusetts. Google Scholar


G. H. Tate 1941. A review of the genus Myotis (Chiroptera) of Eurasia, with special reference to species occurring in the East Indies. Bulletin of the American Museum of Natural History, 78: 537–565. Google Scholar


P. J. Taylor 2000. Bats of Southern Africa. University of Natal Press, Pietermaritzburg, viii + 206 pp. Google Scholar


E. C. Teeling , O. Madsen , R. A. Van Den Bussche , W. W. De Jong , M. J. Stanhope , and M. S. Springer . 2002. Microbat paraphyly and the convergent evolution of a key innovation in Old World rhinolophoid microbats. Proceedings of the National Academy of Sciences of the United States of America, 99: 1431–1436. Google Scholar


O. Thomas 1912. A new vespertilionine bat from Angola. Annals and Magazine of Natural History (Series 8), 10: 204–206 Google Scholar


J. L. Thorne , and H. Kishino . 2002. Divergence time and evolutionary rate estimation with multilocus data. Systematic Biology, 51: 689–702. Google Scholar


J. L. Thorne , H. Kishino , and I. S. Painter . 1998. Estimating the rate of evolution of the rate of molecular evolution. Molecular Biology and Evolution, 15: 1647–1657. Google Scholar


G. Topál 1983. New and rare fossil mouse-eared bats from the Middle Pliocene of Hungary (Mammalia, Chiroptera). Fragmenta Mineralogica et Palaeontologica, 11: 43–54. Google Scholar


M. Volleth , 1992. Comparative analysis of the banded karyotypes of the European Nyctalus species (Vespertilionidae; Chiroptera). Pp. 221–226, in Prague studies in mammalogy ( I. Horáček and V. Vohralík , eds.). Charles University Press, Praha, 246 pp. Google Scholar


M. Volleth , and K.-G. Heller . 1994. Phylogenetic relationships of vespertilionid genera (Mammalia: Chiroptera) as revealed by karyological analysis. Zeitschrift für zoologische Systematik und Evolutionsforschung, 32: 11–34. Google Scholar


M. Volleth , G. Bronner , M. C. Göpfert , K.-G. Heller , O. Von Helversen , and H.-S. Yong . 2001. Karyotype comparison and phylogenetic relationships of Pipistrellus-like bats (Vespertilionidae; Chiroptera; Mammalia). Chromosome Research, 9: 25–46. Google Scholar


O. Von Helversen , K.-G. Heller , F. Mayer , A. Nemeth , M. Volleth , and P. Gombkötö . 2001. Cryptic mammalian species: a new species of whiskered bat (Myotis alcatoe n. sp.) in Europe. Naturwissenschaften, 88: 217–223. Google Scholar


H. Y. Wang , Q. Meiqing , and A. J. Cutler . 1993. A simple method of preparing plant samples for PCR. Nucleic Acids Research, 21: 4153–4154. Google Scholar


H. Yang , E. M. Golenberg , and J. Shoshani . 1997. A blind testing design for authenticating ancient DNA sequences. Molecular Phylogenetics and Evolution, 7: 261–265. Google Scholar


J. Zachos , M. Pagani , L. Sloan , E. Thomas , and K. Billups . 2001. Trends, rhythms, and aberrations in global climate 65 Mya to present. Science, 292: 686–693. Google Scholar


J. Zima , and I. Horáček . 1985. Synopsis of karyotypes of vespertilionid bats (Mammalia: Chiroptera). Acta Universitatis Carolinae (Biologica), 1981: 311–329. Google Scholar


D. J. Zwickl , and D. M. Hillis . 2002. Increased taxon sampling greatly reduces phylogenetic error. Systematic Biology, 51: 588–598. Google Scholar
© Museum and Institute of Zoology PAS
Benoît Stadelmann, David S. Jacobs, Corrie Schoeman, and Manuel Ruedi "Phylogeny of African Myotis Bats (Chiroptera, Vespertilionidae) Inferred from Cytochrome b Sequences," Acta Chiropterologica 6(2), 177-192, (1 December 2004).
Received: 27 August 2004; Accepted: 1 September 2004; Published: 1 December 2004

Back to Top