Journal of Mammalian Evolution

, Volume 9, Issue 1–2, pp 23–53 | Cite as

A Phylogeny of the Neotropical Nectar-Feeding Bats (Chiroptera: Phyllostomidae) Based on Morphological and Molecular Data

  • Bryan C. Carstens
  • Barbara L. Lundrigan
  • Philip Myers


We present a phylogeny of 35 species of nectar-feeding bats based on 119 morphological characters: 62 from the skin, skull, and dentition and 57 soft tissue characters (the latter from Wetterer et al., 2000). These data support monophyly of the subfamilies Brachyphyllinae, Phyllonycterinae, and Glossophaginae, and the tribes Glossophagini and Lonchophyllini. Our analysis contradicts the phylogeny estimated from the RAG-2 gene, which does not support a monophyletic Glossophaginae (Baker et al., 2000). Parsimony analysis of a combined matrix, containing morphological characters and RAG-2 sequences, results in a phylogeny that includes Brachyphyllinae and Phyllonycterinae in Glossophaginae. Support for most clades is stronger than in the morphological tree, but support for basal nodes of the phylogeny remains weak. The weak support at these basal nodes underscores the historical disagreements regarding relationships among these taxa; combining morphological and molecular data has not improved support for these nodes. Uncertainty regarding basal relationships complicates description of morphological change during the evolution of nectarivory in the Phyllostomidae.

Phyllostomidae Glossophaginae Brachyphyllinae Phyllonycterinae nectar-feeding RAG-2 


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  1. Alvarez, J., Willig, M. R., Knox Jones Jr., J., and Webster, W. D. (1991). Glossophaga soricina. Mammal. Species 379: 1–4.Google Scholar
  2. Baker, R. J. (1967). Karyotypes of bats of the family Phyllostomidae and their taxonomic implications. Southwest. Nat. 12: 407–428.Google Scholar
  3. Baker, R. J., and Bass, R. A. (1979). Evolutionary relationships of the Brachyphyllinae to the glossophagine genera Glossophaga and Monophyllus. J. Mammal. 60: 364–372.Google Scholar
  4. Baker, R. J., Honeycutt, R. L., Arnold, M. L., Sarich, V. M., and Genoways, H. H. (1981). Electrophoretic and immunological studies of the relationship of the Brachyphyllinae and the Glossophaginae. J. Mammal. 62: 665–672.Google Scholar
  5. Baker, R. J., Porter, C. A., Patton, J. C., and Van Den Bussche, R. A. (2000). Systematics of the family Phyllostomidae based on RAG-2 DNA sequences. Occ. Pap. Mus. Tex. Tech Univ. 202: 1–16.Google Scholar
  6. Bremer, K. (1988). The limits of amino acid sequence data in angiosperm phylogenetic reconstructions. Evol. 42: 795–803.Google Scholar
  7. Brooks, D. R., and McLennan, D. A. (1991). Phylogeny, Ecology, and Behavior: A Research Program in Comparative Biology. University of Chicago Press, Chicago.Google Scholar
  8. Buzato, S., and Franco, A. L. M. (1992). Tetrastylis ovalis: A second case of bat pollinated passionflower (Passifloraceae). Pl. Syst. Evol. 181: 261–267.Google Scholar
  9. Corbet, G. B., and Hill, J. E. (1980). A World List of Mammalian Species, 1st Edition. London: British Museum.Google Scholar
  10. de la Torre, L. (1961). The evolution, variation, and systematics of the neotropical bats of the genus Sturnira. Ph.D. Diss., Univ. Illinois, Urbana.Google Scholar
  11. Eguiarte, L., and Burquez, A. (1987). Reproductive ecology of Manfreda brachystachya, an iteroparous species of Agavaceae. Southwest. Nat. 32: 169–178.Google Scholar
  12. Felsenstein, J. (1982). Numerical methods for inferring evolutionary trees. Q. Rev. Biol. 57: 379–404.CrossRefGoogle Scholar
  13. Felsenstein, J. (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evol. 39: 783–791.Google Scholar
  14. Fisher, E. A. (1992). Foraging of nectarivorous bats on Bauhinia ungulata. Biotrop. 24: 579–582.Google Scholar
  15. Freeman, P. (1995). Nectarivorous feeding mechanisms in bats. Biol. J. Linn. Soc. 56: 439–463.CrossRefGoogle Scholar
  16. Gardner, A. L. (1977). Chromosomal variation in Vampyressa and a review of chromosomal evolution in the Phyllostomidae (Chiroptera). Syst. Zool. 26: 300–318.Google Scholar
  17. Gibbs, P. E., Oliveira, P. E., and Bianchi, M. B. (1999). Postzygotic control of selfing in Hymenaea stigonocarpa (Leguminosae caesalpinioideae), a bat-pollinated tree of the Brazilian cerrados. Int. J. Plant Sci. 160: 72–78.CrossRefGoogle Scholar
  18. Gimenez, E. D. A., Ferrarezzi, H., and Taddei, V. A. (1996). Lingual morphology and cladistic analysis of the New World nectar-feeding bats (Chiroptera: Phyllostomidae). J. Comp. Biol. 1: 41–64.Google Scholar
  19. Gribel, R., and Hay, J. D. (1993). Pollination ecology of Caryocar brasiliense (Caryocaraceae) in Central Brazil cerrado vegetation. J. Trop. Ecol. 9: 199–211.Google Scholar
  20. Gribel, R., Gibbs, P. E., and De Queiroz, A. L. (1999). Flowering phenology and pollination biology of Ceiba pentandra (Bombaceae) in Central Amazonia. J. Trop. Ecol. 15: 247–253.CrossRefGoogle Scholar
  21. Griffiths, T. A. (1982). Systematics of the new world nectar-feeding bats (Mammalia: Phyllostomidae) based on the morphology of the hyoid and lingual regions. Amer. Mus. Novit. 2742: 1–45.Google Scholar
  22. Griffiths, T. A. (1983). On the phylogeny of the Glossophaginae and the proper use of outgroup analysis. Syst. Zool. 32: 283–285.Google Scholar
  23. Heithaus, E. R., Opler P. A., and Baker, H. G. (1974). Bat activity and pollination of Bauhinia pauletia: Plantpollinator coevolution. Ecol. 55: 412–419.Google Scholar
  24. Heithaus, E. R., Stashko, E., and Anderson, P. K. (1982). Cumulative effects of plant-animal interactions on seed production by Bauhinia ungulata, a Neotropical legume. Ecol. 63: 1294–1302.Google Scholar
  25. Herrera, L. G. M., and Del Rio, C. M. (1998). Pollen digestion by New World Bats: Effects of processing time and feeding habits. Ecol. 79: 2828–2838.Google Scholar
  26. Honeycutt, R. L., and Sarich, V. M. (1987). Albumin evolution and subfamilial relationships among New World leaf-nosed bats (family Phyllostomidae). J. Mammal. 68: 508–517.Google Scholar
  27. Hopkins, H. C. (1984). Floral biology and pollination ecology of the Neotropical species of Parkia. Ecol. 72: 1–23.Google Scholar
  28. Huelsenbeck, J. P., Hillis, D. M., and Jones, R. (1996). Parametric bootstrapping in molecular phylogenetics: Applications and performance. In: Molecular Zoology: Advances, Strategies, and Protocols, J. D. Ferraris and S. R. Palumbi, eds., pp. 519–545, Wiley-Liss, New York, NY.Google Scholar
  29. Jones, J. K., Jr., and Homan, J. A. (1974). Hylonycteris underwoodi. Mammal. Species 32: 1–2.Google Scholar
  30. Koopman, K. (1993). Order Chiroptera. In: Mammal Species of the World, D. E. Wilson and D. M. Reeder, eds., pp. 137–241, Smithsonian Institution Press, Washington, D.C.Google Scholar
  31. Koopman, K. F., and Jones, JR., J. K. (1970). Classification of bats. In: About Bats, B. H. Slaughter and W. D. Walton, eds., pp. 22–28, South. Meth. Univ. Press, Dallas, TX.Google Scholar
  32. Lim, B. K. (1993). Cladistic reappraisal of neotropical stenodermatine bat phylogeny. Cladistics 9: 147–165.CrossRefGoogle Scholar
  33. Luckow, M., and Hopkins, H. C. F. (1995). A cladistic analysis of Parkia (Leguminosae: Mimosoideae). Amer. J. Bot. 82: 1300–1320.Google Scholar
  34. Machado, I. C. S., Sazima, I., and Sazima, M. (1998). Bat pollination of the terrestrial herb Irlbachia alata (Gentianaceae) in northeastern Brazil. Pl. Syst. Evol. 209: 231–237.Google Scholar
  35. Maddison, W. P., and Maddison, D. R. (1992). MacClade: Analysis of Phylogeny and Character Evolution, Version 3.04. Computer program distributed by Sinauer, Sunderland, MA.Google Scholar
  36. McKenna, M. C., and Bell, S. K. (1997). Classification of Mammals above the Species Level. Columbia University Press, New York, NY.Google Scholar
  37. Nellis, D. W., and Ehle, C. P. (1977). Observations on the behavior of Brachyphylla cavernarum (Chiroptera) in Virgin Islands. Mammalia 41: 403–409.Google Scholar
  38. Novak, R.M. (1994). Walker's Mammals of the World, Fifth Edition, Vol. 2. The Johns Hopkins Univ. Press, Baltimore, MD.Google Scholar
  39. Phillips, C. J. (1971). Dentition of glossophagine bats. Univ. Kansas Publ., Mus. of Nat. Hist. 54: 1–138.Google Scholar
  40. Rambaut, A., and Grassly, N. C. (1997). Seq-Gen: An application for the Monte Carlo simulation of DNA sequence evolution along phylogenetic trees. Comp. Applic. Biosci. 13: 235–238.Google Scholar
  41. Ramirez, N., Sobrevila, C., De Enrech, N. X., and Ruiz-Zapata, T. (1984). Floral biology and breeding system of Bauhinia benthamiana taub. (Leguminosae), a bat-pollinated tree in the Venezuelan “Llanos”. Amer J. Bot. 71: 273–280.Google Scholar
  42. Silva-Taboda, G. S., and Pine, R. H. (1969). Morphological and behavioral evidence for the relationship between the bat genus Brachyphylla and the Phyllonycterinae. Biotrop. 1: 10–19.Google Scholar
  43. Simmons, N. B. (1998). A reappraisal of interfamilial relationships of bats. In: Bats: Biology and Conservation, T. H. Kunz and P. A. Racey eds., pp. 3–26, Smithsonian Press, Washington, D. C.Google Scholar
  44. 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. Amer. Mus. Nat. Hist. 235: 1–182.Google Scholar
  45. Simpson, G. G. (1945). The principles of classification and a classification of the mammals. Bull. Amer. Mus. Nat. Hist. 85: 1–350.Google Scholar
  46. Smith, J. D. (1976). Chiropteran evolution. In: Biology of the Bats of the New World Phyllostomidae, Part I., R. J. Baker, J. K. Jones, Jr., and D. C. Carter, eds. Spec. Publ. Mus. Texas Tech Univ. 10: 49–69.Google Scholar
  47. Sorenson, M. D. (1999). TreeRot, version 2. Boston University, Boston MA.Google Scholar
  48. Straney, D. O. (1980). Relationships of Phyllostomatine Bats: Evaluation of Phylogenetic Hypotheses. Ph.D. Diss., Univ. of California, Berkeley.Google Scholar
  49. Sullivan, J. (1996). Combining data with different distributions of among-site rate variation. Syst. Biol. 45: 375–380.Google Scholar
  50. Sullivan, J., Markert, J. A., and Kilpatrick, C. W. (1997). Phylogeography and molecular sytematics of the Peromyscus aztecus species group (Rodentia: Muridae) inferred using parsimony and likelihood. Syst. Biol. 46: 426–440.PubMedGoogle Scholar
  51. Sullivan, J., Arellano, E., and Rogers, D. S. (2000). Comparative phylogeography of Mesoamerican highland rodents: Concerted versus independent responses to past climatic fluctuations. Amer. Nat. 155: 755–768.CrossRefGoogle Scholar
  52. Swofford, D. L. (2002). PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). (PAUP*) Version 4.0b4a. Sinnauer and Associates, Sunderland, MA.Google Scholar
  53. Valiente-Banuet, A. A., Rojas-Martinez, M., Casas, M., Del Coro-Arizmendi, M., and DaVila, P. (1997). Pollination biology of two winter-blooming giant columnar cacti in the Tehuacan Valley, central Mexico. J. Arid Envir. 37: 331–341.CrossRefGoogle Scholar
  54. Voss, R., Turner, M., Inouye, R., Fisher, M., and Cort, R.. (1980). Floral biology of Markea neurantha Hemsley (Solanaceae), a bat-pollinated ephiphyte. Amer. Mid. Nat. 103: 262–268.Google Scholar
  55. Wetterer, A. L., Rockman, M. V., and Simmons, N. B. (2000). Phylogeny of phyllostomid bats (Mammalia: Chiroptera): Data from diverse morphological systems, sex chromosomes, and restriction sites. Bull. Amer. Mus. Nat. Hist. 248: 1–200.CrossRefGoogle Scholar
  56. Wilkinson, M. (1995). A comparison of two methods of character construction. Cladistics 11: 297–308.CrossRefGoogle Scholar
  57. Winkelman, J. R. (1971). Adaptations for Nectar-Feeding in Glossophagine Bats. Ph. D. Diss., Univ. of Michigan, Ann Arbor.Google Scholar
  58. Winter, Y. (1998). Energetic cost of hovering flight in a nectar-feeding bat measured with fast-response respirometry. J. Comp. Physiol. B. 168: 434–444.CrossRefPubMedGoogle Scholar
  59. Winter, Y., Voight, C., and Von Helverson, O. (1998). Gas exchange during hovering flight in a nectar-feeding bat Glossophaga soricina. J. Exper. Biol. 201: 237–244.Google Scholar
  60. Yang, Z., Goldman, N., and Friday, A. (1995). Maximum likelihood trees from DNA sequences: A peculiar statistical estimation problem. Syst. Biol. 44: 384–399.Google Scholar

Copyright information

© Plenum Publishing Corporation 2002

Authors and Affiliations

  • Bryan C. Carstens
    • 1
    • 2
  • Barbara L. Lundrigan
    • 1
  • Philip Myers
    • 3
  1. 1.Michigan State University Museum and Department of ZoologyMichigan State UniversityEast Lansing
  2. 2.The Dept. of Biological SciencesUniversity of IdahoMoscow
  3. 3.Museum of Zoology and Department of Ecology and Evolutionary BiologyUniversity of MichiganAnn Arbor

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