Speciation Dynamics of the Fruit-Eating Bats (Genus Artibeus): With Evidence of Ecological Divergence in Central American Populations

  • Peter A. Larsen
  • María R. Marchán-Rivadeneira
  • Robert J. Baker
Chapter

Abstract

An increasing number of studies have identified complex diversification patterns of Neotropical faunal groups. One example of such complexity is found in bats of the widely distributed and locally abundant Neotropical genus Artibeus, wherein both allopatric and hybrid speciation events have been hypothesized. However, conflicting hypotheses regarding the timescale of diversification for Artibeus exist, and therefore, temporal inferences of the speciation events within the genus remain in doubt. We examine hypotheses regarding the chronology of diversification events within Artibeus. Our results indicate the most parsimonious time of origin for the genus was during the late Miocene to early Pliocene, with multiple speciation events during the early Pleistocene. Considering this evolutionary timescale, we revisit a century-old systematic debate regarding the status of Central American populations known as Artibeus lituratus intermedius. We present nuclear genetic data that indicate intermedius is distinct from lituratus and hypothesize that this distinction was ecologically driven, likely involved sympatry and reinforcement, and occurred during the late Pleistocene or early Holocene. Collectively, the data from Artibeus indicate that multiple speciation processes underlie extant levels of diversity within the genus. Our analyses provide further evidence for complex origins of the Neotropical fauna and contribute to a greater understanding of the natural processes underlying the origin of species.

Keywords

Posit Holocene Miocene Pleistocene Alba 

Notes

Acknowledgments

We thank R. D. Bradley for his valuable discussions throughout the stages of our investigation. C. Blair, H. H. Genoways, S. C. Pedersen, C. D. Phillips, C. J. Phillips, R. E. Strauss, and P. M. Velazco provided helpful comments. We are grateful to H. J. Garner, K. McDonald, and J. P. Carrera of the Natural Science Research Laboratory of the Museum of Texas Tech University for assistance with loans of tissue material. This study would not have been possible were it not for the collecting efforts of members of the 2001 and 2004 Sowell Expeditions to Ecuador and Honduras. We thank all researchers who have worked to generate the molecular data used herein. Financial support was provided by J. Sowell, A. Brown, the Texas Tech University Biological Database Program, and the American Society of Mammalogists.

References

  1. Antonelli A, Nylander JAA, Persson C, Sanmartin I (2009) Tracing the impact of the Andean uplift on Neotropical plant evolution. Proc Natl Acad Sci USA 106(24):9749–9754. doi: 10.1073/pnas.0811421106 PubMedCrossRefGoogle Scholar
  2. Baker RJ, Bininda-Emonds ORP, Mantilla-Meluk H, Porter CA, Van Den Bussche RA (2012) Molecular time scale of diversification of feeding strategy and morphology in New World Leaf-Nosed Bats (Phyllostomidae): a phylogenetic perspective. In: Gunnell GF, Simmons NB (eds) Evolutionary History of Bats: Fossils, Molecules and Morphology. Cambridge Studies in Morphology and Molecules–New Paradigms in Evolutionary Biology. Cambridge University Press, Cambridge, MA, pp 385–409CrossRefGoogle Scholar
  3. Baker RJ, Hoofer SR, Porter CA, Van Den Bussche RA (2003) Diversification among New World leaf-nosed bats: an evolutionary hypothesis and classification inferred from digenomic congruence of DNA sequence. Occas Pap Tex Tech Univ Mus 230:1–32Google Scholar
  4. Beaumont MA, Balding DJ (2004) Identifying adaptive genetic divergence among populations from genome scans. Mol Ecol 13(4):969–980. doi: 10.1111/j.1365-294X.2004.02125.x PubMedCrossRefGoogle Scholar
  5. Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc B-Biol Sci 263(1377):1619–1626. doi: 10.1098/rspb.1996.0237 CrossRefGoogle Scholar
  6. Bininda-Emonds ORP (2007) Fast genes and slow clades: comparative rates of molecular evolution in mammals. Evol Bioinform Online 3:59–85PubMedGoogle Scholar
  7. Brown KS (1976) Geographical patterns of evolution in Neotropical Lepidoptera. Systematics and derivation of known and new Heliconiini (Nymphalidae-Nymphalinae). J Entomol Ser B 44:201–242Google Scholar
  8. Butlin RK (2010) Population genomics and speciation. Genetica 138(4):409–418. doi: 10.1007/s10709-008-9321-3 PubMedCrossRefGoogle Scholar
  9. Cabanne GS, d’Horta FM, Sari EHR, Santos FR, Miyaki CY (2008) Nuclear and mitochondrial phylogeography of the Atlantic forest endemic Xiphorhynchus fuscus (Aves: Dendrocolaptidae): biogeography and systematics implications. Mol Phylogenet Evol 49(3):760–773. doi: 10.1016/j.ympev.2008.09.013 PubMedCrossRefGoogle Scholar
  10. Collins LS, Coates AG, Berggren WA, Aubry MP, Zhang JJ (1996) The late Miocene Panama isthmian strait. Geology 24(8):687–690. doi: 10.1130/0091-7613(1996)024<0687:tlmpis>2.3.co;2 CrossRefGoogle Scholar
  11. Cortes-Ortiz L, Bermingham E, Rico C, Rodriguez-Luna E, Sampaio I, Ruiz-Garcia M (2003) Molecular systematics and biogeography of the Neotropical monkey genus, Alouatta. Mol Phylogenet Evol 26(1):64–81. doi: 10.1016/s1055-7903(02)00308-1 PubMedCrossRefGoogle Scholar
  12. Costa LP (2003) The historical bridge between the Amazon and the Atlantic Forest of Brazil: a study of molecular phylogeography with small mammals. J Biogeogr 30(1):71–86. doi: 10.1046/j.1365-2699.2003.00792.x CrossRefGoogle Scholar
  13. Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland, MAGoogle Scholar
  14. Cracraft J, Prum RO (1988) Patterns and processes of diversification – speciation and historical congruence in some neotropical birds. Evolution 42(3):603–620. doi: 10.2307/2409043 CrossRefGoogle Scholar
  15. Davey JW, Blaxter ML (2011) RADSeq: next-generation population genetics. Brief Funct Genomics 9(5):416–423. doi: 10.1093/bfgp/elq31 Google Scholar
  16. Davis WB (1984) Review of the large fruit-eating bats of the Artibeuslituratus” complex (Chiroptera: Phyllostomidae) in Middle America. Occas Pap Tex Tech Univ Mus 93:1–16Google Scholar
  17. Daza JM, Smith EN, Paez VP, Parkinson CL (2009) Complex evolution in the Neotropics: the origin and diversification of the widespread genus Leptodeira (Serpentes: Colubridae). Mol Phylogenet Evol 53(3):653–667. doi: 10.1016/j.ympev.2009.07.022 PubMedCrossRefGoogle Scholar
  18. Ditchfield AD (2000) The comparative phylogeography of Neotropical mammals: patterns of intraspecific mitochondrial DNA variation among bats contrasted to nonvolant small mammals. Mol Ecol 9(9):1307–1318. doi: 10.1046/j.1365-294x.2000.01013.x PubMedCrossRefGoogle Scholar
  19. Drummond AJ, Nicholls GK, Rodrigo AG, Solomon W (2002) Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 161(3):1307–1320PubMedGoogle Scholar
  20. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214. doi: 10.1186/1471-2148-7-214 PubMedCrossRefGoogle Scholar
  21. Endler JA (1977) Geographic variation, speciation, and clines. Princeton University Press, Princeton, NJGoogle Scholar
  22. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes – application to human mitochondrial-DNA restriction data. Genetics 131(2):479–491PubMedGoogle Scholar
  23. Felsenstein J (1981) Evolutionary trees from DNA-sequences: a maximum-likelihood approach. J Mol Evol 17(6):368–376. doi: 10.1007/bf01734359 PubMedCrossRefGoogle Scholar
  24. Freygang CC (2006) Estudios filogeneticos dos morcegos filostomideos da Regiao Neotropical. PhD Dissertation, Universidade Federal do Rio Grande do SulGoogle Scholar
  25. Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133(3):693–709PubMedGoogle Scholar
  26. Genoways HH, Kwiecinski GG, Larsen PA, Pedersen SC, Larsen RJ, Hoffman JD, de Silva M, Phillips CJ, Baker RJ (2010) Bats of the Grenadine Islands, West Indies, and placement of Koopman’s line. Chiropt Neotrop 16:501–521Google Scholar
  27. Gentry AH (1982) Phytogeographic patterns as evidence for a Choco Refuge. In: Prance GT (ed) Biological diversification in the tropics. Proceedings of the fifth international symposium of the association for tropical biology, Columbia University Press, New York, pp 112–136Google Scholar
  28. Gregory-Wodzicki KM (2000) Uplift history of the Central and Northern Andes: A review. Geol Soc Am Bull 112(7):1091–1105. doi: 10.1130/0016-7606(2000)112<1091:uhotca>2.3.co;2 CrossRefGoogle Scholar
  29. Guerrero JA, de Luna E, González D (2004) Taxonomic status of Artibeus jamaicensis triomylus inferred from molecular and morphometric data. J Mammal 85(5):866–874CrossRefGoogle Scholar
  30. Guerrero JA, Ortega J, González D, Maldonado JE (2008) Molecular phylogenetics and taxonomy of the fruit-eating bats of the genus Artibeus (Chiroptera: Phyllostomidae). In: Lorenzo C, Espinoza E, Ortega J (eds) Avances en el Estudio de los Mamiferos de México. Publicaciones Especiales, vol II. Asociación Mexicana de Mastozoología, A. C., México, D. F., pp 125–146Google Scholar
  31. Haffer J (1967) Speciation in Colombian forest birds west of the Andes. Am Mus Novit 2294:1–57Google Scholar
  32. Haffer J (1969) Speciation in Amazonian forest birds. Science 165:131–137PubMedCrossRefGoogle Scholar
  33. Hendry AP, Nosil P, Rieseberg LH (2007) The speed of ecological speciation. Funct Ecol 21(3):455–464. doi: 10.1111/j.1365-2435.2006.01240.x PubMedCrossRefGoogle Scholar
  34. Ho SYW (2007) Calibrating molecular estimates of substitution rates and divergence times in birds. J Avian Biol 38(4):409–414. doi: 10.1111/j.2007.0908-8857.04168.x Google Scholar
  35. Hoffmann FG, Baker RJ (2001) Systematics of bats of the genus Glossophaga (Chiroptera: Phyllostomidae) and phylogeography in G. soricina based on the cytochrome-b gene. J Mammal 82(4):1092–1101. doi: 10.1644/1545-1542(2001)082<1092:sobotg>2.0.co;2 CrossRefGoogle Scholar
  36. Hoffmann FG, Baker RJ (2003) Comparative phylogeography of short-tailed bats (Carollia: Phyllostomidae). Mol Ecol 12(12):3403–3414. doi: 10.1046/j.1365-294X.2003.02009.x PubMedCrossRefGoogle Scholar
  37. Hoofer SR, Solari S, Larsen PA, Bradley RD, Baker RJ (2008) Phylogenetics of the fruit-eating bats (Phyllostomidae: Artibeina) inferred from mitochondrial DNA sequences. Occas Pap Tex Tech Univ Mus 277:1–15Google Scholar
  38. Hooghiemstra H, van der Hammen T (1998) Neogene and quaternary development of the neotropical rain forest: the forest refugia hypothesis, and a literature overview. Earth-Sci Rev 44(3–4):147–183. doi: 10.1016/s0012-8252(98)00027-0 CrossRefGoogle Scholar
  39. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8):754–755. doi: 10.1093/bioinformatics/17.8.754 PubMedCrossRefGoogle Scholar
  40. Hughes C, Eastwood R (2006) Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. Proc Natl Acad Sci USA 103(27):10334–10339. doi: 10.1073/pnas.0601928103 PubMedCrossRefGoogle Scholar
  41. Jones KE, Bininda-Emonds ORP, Gittleman JL (2005) Bats, clocks, and rocks: diversification patterns in chiroptera. Evolution 59(10):2243–2255. doi: 10.1554/04-635.1 PubMedGoogle Scholar
  42. Keigwin L (1982) Isotopic paleoceanography of the Caribbean and East pacific: role of Panama uplift in late neogene time. Science 217:350–353PubMedCrossRefGoogle Scholar
  43. Kirby MX, Jones DS, MacFadden BJ (2008) Lower miocene stratigraphy along the Panama Canal and its bearing on the Central American Peninsula. PLoS One 3(7):e2791. doi: 10.1371/journal.pone.0002791 PubMedCrossRefGoogle Scholar
  44. Lack JB, Pfau RS, Wilson GM (2010) Demographic history and incomplete lineage sorting obscure population genetic structure of the Texas mouse (Peromyscus attwateri). J Mammal 91(2):314–325. doi: 10.1644/09-mamm-a-242.1 CrossRefGoogle Scholar
  45. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X version 2.0. Bioinformatics 23(21):2947–2948. doi: 10.1093/bioinformatics/btm404 PubMedCrossRefGoogle Scholar
  46. Larsen PA, Hoofer SR, Bozeman MC, Pedersen SC, Genoways HH, Phlllips CJ, Pumo DE, Baker RJ (2007) Phylogenetics and phylogeography of the Artibeus jamaicensis complex based on cytochrome-b DNA sequences. J Mammal 88(3):712–727. doi: 10.1644/06-mamm-a-125r.1 CrossRefGoogle Scholar
  47. Larsen PA, Marchan-Rivadeneira MR, Baker RJ (2010a) Taxonomic status of Andersen’s fruit-eating bat (Artibeus jamaicensis aequatorialis) and revised classification of Artibeus (Chiroptera: Phyllostomidae). Zootaxa 2648:45–60Google Scholar
  48. Larsen PA, Marchan-Rivadeneira MR, Baker RJ (2010b) Natural hybridization generates mammalian lineage with species characteristics. Proc Natl Acad Sci USA 107(25):11447–11452. doi: 10.1073/pnas.1000133107 PubMedCrossRefGoogle Scholar
  49. Lessa EP, Cook JA, Patton JL (2003) Genetic footprints of demographic expansion in North America, but not Amazonia, during the late quaternary. Proc Natl Acad Sci USA 100(18):10331–10334. doi: 10.1073/pnas.1730921100 PubMedCrossRefGoogle Scholar
  50. Leyden BW (1984) Guatemalan forest synthesis after Pleistocene aridity. Proc Natl Acad Sci USA 81(15):4856–4859. doi: 10.1073/pnas.81.15.4856 PubMedCrossRefGoogle Scholar
  51. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451–1452. doi: 10.1093/bioinformatics/btp187 PubMedCrossRefGoogle Scholar
  52. Lim BK (1997) Morphometric differentiation and species status of the allopatric fruit-eating bats Artibeus jamaicensis and A. planirostris in Venezuela. Stud Neotrop Fauna E 32(2):65–71. doi: 10.1080/01650521.1997.9709606 Google Scholar
  53. Lim BK, Engstrom MD, Lee TE, Patton JC, Bickham JW (2004) Molecular differentiation of large species of fruit-eating bats (Artibeus) and phylogenetic relationships based on the cytochrome-b gene. Acta Chiropterol 6(1):1–12CrossRefGoogle Scholar
  54. Maddison DR, Maddison WP (2000) MacClade 4: analysis of phylogeny and character evolution. Version 4.0. Sinauer Associates, Sunderland, MAGoogle Scholar
  55. Mallet J, Beltran M, Neukirchen W, Linares M (2007) Natural hybridization in heliconiine butterflies: the species boundary as a continuum. BMC Evol Biol 7:28. doi: 10.1186/1471-2148-7-28 PubMedCrossRefGoogle Scholar
  56. Marchán-Rivadeneira MR, Larsen PA, Phillips CJ, Strauss RE, Baker RJ (2012) On the association between environmental gradients and skull size variation in the great fruit-eating bat, Artibeus lituratus (Chiroptera: Phyllostomidae). Biol J Linn Soc 105(3):623–634. doi: 10.1111/j.1095-8312.2011.01804.x CrossRefGoogle Scholar
  57. Martins FM, Ditchfield AD, Meyer D, Morgante JS (2007) Mitochondrial DNA phylogeography reveals marked population structure in the common vampire bat, Desmodus rotundus (Phyllostomidae). J Zoolog Syst Evol Res 45(4):372–378. doi: 10.1111/j.1439-0469.2007.00419.x CrossRefGoogle Scholar
  58. Marques-Aguiar SA (2007) Genus Artibeus Leach, 1821. In: Gardner AL (ed) Mammals of South America, vol 1. University of Chicago Press, Chicago, IL, pp 301–321Google Scholar
  59. Mavárez J, Salazar CA, Bermingham E, Salcedo C, Jiggins CD, Linares M (2006) Speciation by hybridization in Heliconius butterflies. Nature 441(7095):868–871. doi: 10.1038/nature04738 PubMedCrossRefGoogle Scholar
  60. Miller MP (2005) Alleles In Space (AIS): computer software for the joint analysis of interindividual spatial and genetic information. J Hered 96(6):722–724. doi: 10.1093/jhered/esi119 PubMedCrossRefGoogle Scholar
  61. Monmonier M (1973) Maximum-difference barriers: an alternative numerical regionalization method. Geogr Anal 3:245–261Google Scholar
  62. Moritz C, Patton JL, Schneider CJ, Smith TB (2000) Diversification of rainforest faunas: an integrated molecular approach. Annu Rev Ecol Syst 31:533–563. doi: 10.1146/annurev.ecolsys.31.1.533 CrossRefGoogle Scholar
  63. Noonan BP, Gaucher P (2006) Refugial isolation and secondary contact in the dyeing poison frog Dendrobates tinctorius. Mol Ecol 15(14):4425–4435. doi: 10.1111/j.1365-294X.2006.03074.x PubMedCrossRefGoogle Scholar
  64. Orr MR, Smith TB (1998) Ecology and speciation. Trends Ecol Evol 13(12):502–506. doi: 10.1016/s0169-5347(98)01511-0 PubMedCrossRefGoogle Scholar
  65. Patten DR (1971) A review of the large species of Artibeus (Chiroptera: Phyllostomidae) from western South America. PhD Dissertation, Texas A&M UniversityGoogle Scholar
  66. Patterson BD, Pacheco V, Ashley MV (1992) On the origins of the western slope region of endemism: systematics of fig eating bats, genus Artibeus. Memorias del Museo de Historia Natural, Universidad Nacional Mayor de San Marcos (Lima) 21:189–205Google Scholar
  67. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6(1):288–295. doi: 10.1111/j.1471-8286.2005.01155.x CrossRefGoogle Scholar
  68. Pennington RT, Prado DE, Pendry CA (2000) Neotropical seasonally dry forests and quaternary vegetation changes. J Biogeogr 27(2):261–273CrossRefGoogle Scholar
  69. Piperno DR, Jones JG (2003) Paleoecological and archaeological implications of a Late Pleistocene/Early Holocene record of vegetation and climate from the Pacific coastal plain of Panama. Quat Res 59(1):79–87. doi: 10.1016/s0033-5894(02)00021-2 CrossRefGoogle Scholar
  70. Porter CA, Baker RJ (2004) Systematics of Vampyressa and related genera of phyllostomid bats as determined by cytochrome-b sequences. J Mammal 85(1):126–132. doi: 10.1644/bwg-110 CrossRefGoogle Scholar
  71. Porter CA, Hoofer SR, Cline CA, Hoffmann FG, Baker RJ (2007) Molecular phylogenetics of the phyllostomid bat genus Micronycteris with descriptions of two new subgenera. J Mammal 88(5):1205–1215. doi: 10.1644/06-mamm-a-292r.1 CrossRefGoogle Scholar
  72. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14(9):817–818. doi: 10.1093/bioinformatics/14.9.817 PubMedCrossRefGoogle Scholar
  73. Prance GT (1982) Forest refuges: evidence from woody angiosperms. In: Prance GT (ed) Biological diversification in the tropics. Proceedings of the fifth international symposium of the association for tropical biology, Columbia University Press, New York, pp 137–156Google Scholar
  74. Redondo RAF, Brina LPS, Silva RF, Ditchfield AD, Santos FR (2008) Molecular systematics of the genus Artibeus (Chiroptera: Phyllostomidae). Mol Phylogenet Evol 49(1):44–58. doi: 10.1016/j.ympev.2008.07.001 PubMedCrossRefGoogle Scholar
  75. Rheindt FE, Christidis L, Cabanne GS, Miyaki C, Norman JA (2009) The timing of neotropical speciation dynamics: a reconstruction of Myiopagis flycatcher diversification using phylogenetic and paleogeographic data. Mol Phylogenet Evol 53(3):961–971. doi: 10.1016/j.ympev.2009.09.001 PubMedCrossRefGoogle Scholar
  76. Rice AM, Rudh A, Ellegren H, Qvarnstrom A (2011) A guide to the genomics of ecological speciation in natural animal populations. Ecol Lett 14(1):9–18. doi: 10.1111/j.1461-0248.2010.01546.x PubMedCrossRefGoogle Scholar
  77. Rogers AR, Harpending H (1992) Population-growth makes waves in the distribution of pairwise genetic-differences. Mol Biol Evol 9(3):552–569PubMedGoogle Scholar
  78. Rull V (2008) Speciation timing and neotropical biodiversity: the tertiary-quaternary debate in the light of molecular phylogenetic evidence. Mol Ecol 17(11):2722–2729. doi: 10.1111/j.1365-294X.2008.03789.x PubMedCrossRefGoogle Scholar
  79. Rundle HD, Nosil P (2005) Ecological speciation. Ecol Lett 8(3):336–352. doi: 10.1111/j.1461-0248.2004.00715.x CrossRefGoogle Scholar
  80. Santos JC, Coloma LA, Summers K, Caldwell JP, Ree R, Cannatella DC (2009) Amazonian amphibian diversity is primarily derived from late Miocene Andean lineages. PLoS Biol 7(3):448–461. doi: 10.1371/journal.pbio.1000056 CrossRefGoogle Scholar
  81. Simmons NB (2005) Order Chiroptera. In: Wilson DE, Reeder DM (eds) Mammals species of the world: a taxonomic and geographic reference, 3rd edn. Johns Hopkins University Press, Baltimore, MD, pp 312–529Google Scholar
  82. Smith BT, Klicka J (2010) The profound influence of the Late Pliocene Panamanian uplift on the exchange, diversification, and distribution of New World birds. Ecography 33(2):333–342. doi: 10.1111/j.1600-0587.2009.06335.x Google Scholar
  83. Solari S, Hoofer SR, Larsen PA, Brown AD, Bull RJ, Guerrero JA, Ortega J, Carrera JP, Bradley RD, Baker RJ (2009) Operational criteria for genetically defined species: analysis of the diversification of the small fruit-eating bats, Dermanura (Phyllostomidae: Stenodermatinae). Acta Chiropterol 11(2):279–288. doi: 10.3161/150811009x485521 CrossRefGoogle Scholar
  84. Stadelmann B, Lin LK, Kunz TH, Ruedi M (2007) Molecular phylogeny of New World Myotis (Chiroptera, Vespertilionidae) inferred from mitochondrial and nuclear DNA genes. Mol Phylogenet Evol 43(1):32–48. doi: 10.1016/j.ympev.2006.06.019 PubMedCrossRefGoogle Scholar
  85. Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (* and other methods). Version 4.0b10. Sinauer Associates Inc., Sunderland, MAGoogle Scholar
  86. Tajima F (1989) Statistical-method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3):585–595PubMedGoogle Scholar
  87. Teeling EC, Springer MS, Madsen O, Bates P, O'Brien SJ, Murphy WJ (2005) A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307(5709):580–584. doi: 10.1126/science.1105113 PubMedCrossRefGoogle Scholar
  88. Van Den Bussche RA, Hudgeons JL, Baker RJ (1998) Phylogenetic accuracy, stability, and congruence. Relationships within and among the New World bat genera Artibeus, Dermanura, and Koopmania. In: Kunz TH, Racey PA (eds) Bat biology and conservation. Smithsonian Institution Press, Washington, DC, pp 59–71Google Scholar
  89. Velazco PM, Patterson BD (2008) Phylogenetics and biogeography of the broad-nosed bats, genus Platyrrhinus (Chiroptera: Phyllostomidae). Mol Phylogenet Evol 49(3):749–759. doi: 10.1016/j.ympev.2008.09.015 PubMedCrossRefGoogle Scholar
  90. Webster D, Jones JK (1983) Artibeus hirsutus and Artibeus inopinatus. Mammal Species 199:1–3CrossRefGoogle Scholar
  91. Weir JT (2006) Divergent timing and patterns of species accumulation in lowland and highland Neotropical birds. Evolution 60(4):842–855PubMedGoogle Scholar
  92. Wesselingh FP, Salo JA (2006) A Miocene perspective on the evolution of the Amazonian biota. Scripta Geol 133:439–458Google Scholar
  93. Wilson DE (1991) Mammals of the Tres-Marias Islands. Bull Am Mus Nat Hist 206:214–250Google Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Peter A. Larsen
    • 1
  • María R. Marchán-Rivadeneira
    • 2
  • Robert J. Baker
    • 2
  1. 1.Department of BiologyDuke UniversityDurhamUSA
  2. 2.Department of Biological SciencesTexas Tech UniversityLubbockUSA

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