Abstract
Molecular and morphological analyses of variation often conflict with historical species descriptions based on a few characters and small samples sizes. Here we present a molecular phylogeny together with a quantitative morphological analysis of the species in Sturnira in Ecuador. The 438 terminal taxa or organisms included in the anlaysis occur within a total of 10 ingroup lineages, which contain considerable substructure. Some species, as recognized by their morphological traits, form paraphyletic arrangements with other taxa. We could not distinguish the close species pairs S. erythromos / S. bogotensis and S. ludovici / S. oporophilum in morphospace and therefore when distinct lineages were recovered genetically, they initially contained mixed membership of specimens identified using morphological criteria. Similarly, the qualitative character states that diagnose S. luisi in its original description are not recovered in a quantitative analysis of morphological variation and thus S. luisi cannot be mapped to a single lineage in a molecular phylogeny. We present additional evidence to corroborate the existence of S. perla as a species. We found a remarkable geographic structure within some species containing sister pairings, with lineages having a clear eastern or western distribution in relation to theAndes. Our analysis demonstrates the potential for conflict between character-based diagnoses, analysis of morphological variation and molecular phylogenetics in the identification of species and supports a combined approach to this problem.
References
Agnarsson, I., Zambrana-Torrelio, C.M., Flores-Saldana, N.P., & May-Collado, L.J. (2011) A time-calibrated species-level phylogeny of bats (Chiroptera, Mammalia). PLoS Currents: Tree of life, 3, RRN1212.
Albuja, V.L. (1999) Murciélagos del Ecuador. 2nd edition. Cicetrónic Cía Ltda, Offset, Quito, Ecuador, 288 pp.
Anthony, H.E. (1924) Preliminary report on Ecuadorean mammals. No. 6. American Museum Novitates, 139, 1–9.
Borisenko, A.V., Lim, B.K., Ivvanova, N.V., Hanner, R.H. & Hebert, P.D.N. (2008) DNA barcoding in surveys of small mammal communities: a field study in Suriname. Molecular Ecology Resources, 8, 471–479.
http://dx.doi.org/10.1111/j.1471-8286.2007.01998.xBrumfield, R.T. & Capparella, A.P. (1996) Historical diversification of birds in northwestern South America: A molecular perspective on the role of vicariant events. Evolution, 50, 1607–1624.
http://dx.doi.org/10.2307/2410897Brumfield, R.T. & Edwards, S.V. (2007) Evolution into and out of the Andes: a Bayesian analysis of historical diversification in Thamnophilus antshrikes. Evolution, 61, 346-367.
http://dx.doi.org/10.1111/j.1558-5646.2007.00039.xClare, E.L. (2011) Cryptic Species? Patterns of maternal and paternal gene flow in eight neotropical bats. PLoS ONE, 6, e21460.
http://dx.doi.org/10.1371/journal.pone.0021460Clare, E.L., Lim, B.K., Engstrom, M.D., Eger, J.L. & Hebert, P.D.N. (2007) DNA barcoding of Neotropical bats: species identification and discovery within Guyana. Molecular Ecology Notes, 7, 184–190.
http://dx.doi.org/10.1111/j.1471-8286.2006.01657.xDavis, W.B. (1980) New Sturnira (Chiroptera: Phyllostomidae) from Central and South America, with key to currently recognized species. Occasional Papers Museum Texas Tech University, 70, 1–5.
de la Torre, L. (1959) A new species of bat of the genus Sturnira (Phyllostomidae) from the Island of Trinidad, West Indies. Natural History Miscellanea Chicago Academy of Sciences, 166, 1–6.
Dobzhansky, T. (1937) Genetics and the Origin of Species. Second Edition. Columbia University Press, New York, 364 pp.
Dryden, I.L. & Mardia, K.V. (1998) Multivariate shape analysis. Sankhya, 55, 460–480.
Eisenberg, J.F. & Redford, K.H. (1999) Mammals of the Neotropics. The Central Neotropics. Volume 3. The University of Chicago Press, Chicago, 609 pp.
Gardner, A.L. (2008) Tribe Sturnirini. In: Gardner, A.L. (Ed.), Mammals of South America. Volume 1: Marsupials, Xenarthrans, Shrews, and Bats. The University of Chicago Press, Chicago, pp. 363–376.
Guindon, S. & Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704.
http://dx.doi.org/10.1080/10635150390235520Hajibabaei, M., deWaard, J.R., Ivanova, N.V., Ratnasingham, S., Dooh, R.T., Kirk, S.L., Mackie, P.M. & Hebert, P.D.N. (2005) Critical factors for assembling a high volume of DNA barcodes. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences, 360, 1959–1967.
http://dx.doi.org/10.1098/rstb.2005.1727Hey, J. (2001) The mind of the species problem. Trends in Ecology and Evolution, 16, 326–329.
http://dx.doi.org/10.1016/S0169-5347(01)02145-0Hebert, P.D.N., Cywinska, A., Ball, S.L. & deWaard, J.R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London, Series B, Biological Sciences, 270, 313–321.
http://dx.doi.org/10.1098/rspb.2002.2218Hoffmann, F.G. & Baker, R.J. (2001) Systematics of bats of the genus Glossophaga Chiroptera: Phyllostomidae and phylogeography in G. soricina based on the Cytochrome-b gene. Journal of Mammalogy, 84, 1092–1101.
http://dx.doi.org/10.1644/1545-1542(2001)082<1092:SOBOTG>2.0.CO;2Hoffmann, F.G. & Baker, R.J. (2003) Comparative phylogeography of short-tailed bats (Carollia: Phyllostomidae). Molecular Ecology, 12, 3403–3414.
http://dx.doi.org/10.1046/j.1365-294X.2003.02009.xHuelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics, 17, 754–755.
http://dx.doi.org/10.1093/bioinformatics/17.8.754Hull, D.L. (1965) The Effect of Essentialism on Taxonomy--Two Thousand Years of Stasis (I). The British Journal for the Philosophy of Science, 15, 314–326.
http://dx.doi.org/10.1093/bjps/XV.60.314Hull, D.L. (1976) Are species really individuals? Systematic Zoology, 25, 174–191.
http://dx.doi.org/10.2307/2412744Humphries, E.M. & Winker, K. (2010) Working through polytomies: Auklets revisited. Molecular Phylogenetics and Evolution, 54, 88–96.
http://dx.doi.org/10.1016/j.ympev.2009.07.023Iudica, C.A. (2000) Systematic revision of the neotropical fruit bats of the genus Sturnira: A molecular and morphological approach. PhD dissertation thesis. University of Florida. Gainesville, USA, 284 pp.
Ivanova, N.V., deWaard, J.R. & Hebert, P.D.N. (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes, 6, 998–1002.
http://dx.doi.org/10.1111/j.1471-8286.2006.01428.xIvanova, N.V., Zemlak, T.S., Hanner, R.H. & Hebert, P.D.N. (2007) Universal primer cocktails for fish DNA barcoding. Molecular Ecology Notes, 7, 544–548.
http://dx.doi.org/10.1111/j.1471-8286.2007.01748.xIvanova, N.V., Clare, E.L. & Borisenko, A.V. (2012) DNA barcoding mammals. In: Kress, W.J. & Erickson, D.L. (Eds), DNA Barcodes : Methods and Protocols, Methods in Molecular Biology vol. 858, pp. 153-182.
http://dx.doi.org/10.1007/978-1-61779-591-6_8Ives, A.R., Midford, P.E. & Garland, Jr., T. (2007) Within-species variation and measurement error in phylogenetic comparative methods. Systematic Biology, 56, 252– 270.
http://dx.doi.org/10.1080/10635150701313830Jarrín-V., P. (2012) Species boundaries in bats. a philosophical, morphometric, environmental and phylogenetic essay in the genera Anoura, Carollia and Sturnira. Ph. D. Dissertation thesis. Boston University, Boston, USA, 342 pp.
Jarrín-V., P., Flores-C., C. & Salcedo-Q, J. (2010) Morphological variation in the Short-tailed Fruit Bat (Carollia) in Ecuador, with comments on the practical and philosophical aspects of boundaries among species. Integrative Zoology, 5, 226–240.
http://dx.doi.org/10.1111/j.1749-4877.2010.00208.xJarrín-V., P. & Kunz, T.H. (2011) A new species of Sturnira (Chiroptera: Phyllostomidae) from the Choco forest of Ecuador. Zootaxa, 2755, 1–35.
Jarrín-V., P. & Menendez-Guerrero, P.A. (2011) Environmental components and boundaries of morphological variation in the short-tailed fruit bat (Carollia spp.) in Ecuador. Acta Chiropterologica, 13, 319–340.
http://dx.doi.org/10.3161/150811011X624802Jarrín-V., P. & Coello, D. (2012) Morphological variation in Anoura fistulata (Chiroptera: Phyllostomidae) relative to conspecific and sympatric species in Ecuador. Acta Chiropterologica, 14, 317–333.
Lattin, J., Carroll, J.D. & Green, P.E. (2003) Analyzing Multivariate Data. Thomson Learning, Toronto, Canada, 556 pp.
Marinkelle, C.J. & Cadena, A. (1971) Remarks on Sturnira tildae in Colombia. Journal of Mammalogy, 52, 235–237.
http://dx.doi.org/10.2307/1378460Mayr, E. (1959) Typological versus Population Thinking. In: Meggers, B.J. (Ed.), Evolution and Anthropology: A Centennial Appraisal. The Anthropological Society of Washington, Washington, pp. 1–10.
http://dx.doi.org/10.1016/0076-6879(83)01005-8Messing, J. (1983) New M13 vectors for cloning. Methods in Enzymology, 101, 20–78.
Miretzki, M. (2002) Southernmost records of Sturnira tildae de la Torre, 1959 (Chiroptera: Phyllostomidae) in Brazil. Mammalia, 66, 306–309.
Muñoz, J. (2001) Murciélagos de Colombia, sistemática, distribución,descripción, historia natural y ecología. Editorial Universidad de Antioquia, Medellín, 391 pp.
Myers, N., Mittermeier, R.A., Mittermeier, C.G., da Fonseca, G.A.B. & Kent, J. (2000) Biodiversity hotspots for conservation priorities. Nature, 403, 853–858.
http://dx.doi.org/10.1038/35002501Pacheco, V. & Patterson, B.D. (1991) Phylogeny relationships of the New World bat genus Sturnira (Chiroptera: Phyllostomidae). Bulletin of the American Museum of Natural History, 206, 101–121.
Pfunder, M., Holzgang, O. & Frey, J.E. (2004) Development of microarray based diagnostics of voles and shrews for use in biodiversity monitoring studies, and evaluation of mitochondrial cytochrome oxidase I vs. cytochrome b as genetic markers. Molecular Ecology, 13, 1277–1286.
http://dx.doi.org/10.1111/j.1365-294X.2004.02126.xPinto, C.M. (2009) Genetic diversity of the Common Vampire Bat Desmodus rotundus in Ecuador: testing cross-Andean gene flow. MA dissertation thesis. Texas Tech University. Texas, USA, 60 pp.
Posada, D. (2008) jModelTest: Phylogenetic Model Averaging. Molecular Biology and Evolution, 25, 1253–1256.
http://dx.doi.org/10.1093/molbev/msn083Rohlf, F.J. (1993) Relative warp analysis and an example of its application to the analysis of mosquito wings. In: Marcus, L.F., Bello, E. & García Valdecasas, A. (Eds), Contributions to Morphometrics. Museo Nacional de Ciencias Naturales (CSIC), Volume 8, Madrid, Spain, pp. 131–159.
Rohlf, F.J. & Bookstein, F.L. (2003) Computing the uniform component of shape variation. Systematic Biology, 52, 66–69.
http://dx.doi.org/10.1080/10635150390132759Ron, S.R. (2000) Biogeographic area relationships of lowland Neotropical rainforest based on raw distributions of vertebrate groups. Biological Journal of the Linnean Society, 71, 379–402.
http://dx.doi.org/10.1111/j.1095-8312.2000.tb01265.xRonquist, F. & Huelsenbeck, J.P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.
http://dx.doi.org/10.1093/bioinformatics/btg180Rubinoff, D. & Holland, B.S. (2005) Between Two Extremes: Mitochondrial DNA is neither the Panacea nor the Nemesis of Phylogenetic and Taxonomic Inference. Systematic Biology, 54, 952–961.
http://dx.doi.org/10.1080/10635150500234674Schulte, J.A.II., Macey, J.R., Espinoza, R.E. & Larson, A. (2000). Phylogenetic relationships in the iguanid lizard genus Liolaemus: multiple origins of viviparous reproduction and evidence for recurring Andean vicariance and dispersal. Biological Journal of the Linnean Society, 69, 75–102.
http://dx.doi.org/10.1006/bijl.1999.0346Shamel, H.H. (1927) A new bat from Colombia. Proceedings of the Biological Society of Washington, 40, 129–130.
Simmons, N.B. (2005) Order Chiroptera. In: Wilson, D.E. & Reeder, D.M. (Eds.), Mammal species of the world, a taxonomic and geographic reference. 3rd edition. Smithsonian Institution Press, Washington D.C., pp. 312–529.
Stamatakis, A. (2006) RAxML-VI-HPC: Maximum likelihood-based phylognetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690.
http://dx.doi.org/10.1093/bioinformatics/btl446Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Molecular Biology and Evolution, 28, 2731–2739.
http://dx.doi.org/10.1093/molbev/msr121Tirira, D.S. (1999) Mamíferos del Ecuador. Publicación Especial, Museo de Zoología, Centro de Biodiversidad y Ambiente, Pontificia Universidad Católica del Ecuador, 2, 1–392.
Tschudi, P.P. (1844) Untersuchimgen über die Fauna Peruana. St. Gallen, Sweden, 262 pp.
Villalobos, F. & Valerio, A.A. (2002) The phylogenetic relationships of the bat genus Sturnira Gray, 1842 (Chiroptera: Phyllostomidae). Mammalian Biology, 67, 268–275.
http://dx.doi.org/10.1078/1616-5047-00041Will, K.W. & Rubinoff, D. (2004) Myth of the molecule: DNA barcodes for species cannot replace morphology for identification and classification. Cladistics, 20, 47−55.
http://dx.doi.org/10.1111/j.1096-0031.2003.00008.x