DNA barcoding of bats (Chiroptera) from the Colombian northern region
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Álvaro J. Benítez
, Dina Ricardo-Caldera
, María Atencia-Pineda
und Richard Hoyos-López
Abstract
Bats are mammals of great ecological and medical importance, which have associations with different pathogenic microorganisms. DNA barcoding is a tool that can expedite species identification using short DNA sequences. In this study, we assess the DNA barcoding methodology in bats from the Colombian Northern region, specifically in the Córdoba department. Cytochrome oxidase subunit I (COI) gene sequences of nine bat species were typified, and their comparison with other Neotropic samples revealed that this marker is suitable for individual species identification, with ranges of intra-species variation from 0.1 to 0.9%. Bat species clusters are well supported and differentiated, showing average genetic distances ranging from 3% between Artibeus lituratus and Artibeus planirostris, up to 27% between Carollia castanea and Molossus molossus. C. castanea and Glossophaga soricina show geographical structuring in the Neotropic. The findings reported in this study confirm DNA barcoding usefulness for fast species identification of bats in the region.
Funding source: Córdoba Government, the General System of Royalties
Award Identifier / Grant number: 754/2013
Funding source: Universidad del Sinú – Elías Bechara Zainúm
Funding source: Universidad de Córdoba
Acknowledgments
The authors would like to thank the Molecular Biology and Biomedical Science Laboratory from Universidad del Sinú, for its support in accomplishing the molecular protocols, as well as the people who collaborated in the field phase. The authors would like to give special thanks to Josef Bryja, Héctor Ramírez, and two anonymous reviewers for their valuable comments on the manuscript.
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Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
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Research funding: This work was funded by the Córdoba Government, the General System of Royalties (SGR, for its acronym in Spanish), Colombia (grant no. 754/2013), Universidad del Sinú – Elías Bechara Zainúm (UNISINÚ) and Universidad de Córdoba.
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Conflict of interest statement: The authors declare that they have no conflicts of interest regarding this article.
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Research ethics: All the methods used in this study were approved by the Health Sciences Faculty Ethics’ Committee from Universidad del Sinú (Act No 01 of 2017), following the ethical guidelines established by the American Society of Mammalogists for specimens euthanasia (Sikes and The Animal Care and Use Committee of the American Society of Mammalogists 2016). The collection was carried out under the permission of the National Authority of Environmental Licenses for Universidad de Córdoba, through resolution 00914 (August 4th, 2017), to conduct scientific research without commercial purposes in wild animals. Specimens were deposited in the zoological collection from Universidad de Córdoba (CZUC). All sequences were registered on GenBank under the following accession numbers: from MK749466 to MK749564.
References
Arenas-Viveros, D., Sánchez-Vendizú, P., Giraldo, A., and Salazar-Bravo, J. (2021). A new species of Cynomops (Chiroptera: Molossidae) from the northwestern slope of the Andes. Mammalia 85: 273–286, doi:10.1515/mammalia-2020-0068.10.1515/mammalia-2020-0068Suche in Google Scholar
Barnosky, A.D., Matzke, N., Tomiya, S., Wogan, G.O.U., Swartz, B., Quental, T.B., Marshall, C., Mcguire, J.L., Lindsey, E.L., Maguire, K.C., et al.. (2011). Has the Earth’s sixth mass extinction already arrived? Nature 471: 51–57, https://doi.org/10.1038/nature09678.Suche in Google Scholar PubMed
Borisenko, A.V., Lim, B.K., Ivanova, N.V., Hanner, R.H., and Hebert, P.D.N. (2008). DNA barcoding in surveys of small mammal communities: a field study in Suriname. Mol. Ecol. Resour. 8: 471–479, https://doi.org/10.1111/j.1471-8286.2007.01998.x.Suche in Google Scholar PubMed
Bouckaert, R., Heled, J., Kuhnert, D., Vaughan, T., Wu, C., Xie, D., Suchard, M.A., Rambaut, A., and Drummond, A.J. (2014). BEAST 2 : a software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 10: e1003537, https://doi.org/10.1371/journal.pcbi.1003537.Suche in Google Scholar PubMed PubMed Central
Ceballos, G., Ehrlich, P.R., and Dirzo, R. (2017). Biological annihilation via the ongoing sixth mass extinction signaled by vertebrate population losses and declines. Proc. Natl. Acad. Sci. 114: E6089–E6096, https://doi.org/10.1073/pnas.1704949114.Suche in Google Scholar PubMed PubMed Central
Chacón, J., Ballesteros, J., and Racero-Casarrubia, J. (2018). Nuevos registros de Pteronotus parnellii (Chiroptera, Mormoopidae) en el departamento de Córdoba, Colombia. Bol. Científico Cent. Museos Mus. Hist. Nat. 22: 121–127.10.17151/bccm.2018.22.1.11Suche in Google Scholar
Clare, E.L. (2011). Cryptic species? Patterns of maternal and paternal gene flow in eight Neotropical bats. PloS One 6: e21460, https://doi.org/10.1371/journal.pone.0021460.Suche in Google Scholar PubMed PubMed Central
Clare, E.L., Lim, B.K., Engstrom, M.D., Eger, J.L., and Hebert, P.D.N. (2007). DNA barcoding of Neotropical bats: species identification and discovery within Guyana: barcoding. Mol. Ecol. Notes 7: 184–190, https://doi.org/10.1111/j.1471-8286.2006.01657.x.Suche in Google Scholar
Clare, E.L., Lim, B.K., Fenton, M.B., and Hebert, P.D.N. (2011). Neotropical bats: estimating species diversity with DNA barcodes. PloS One 6: e22648, https://doi.org/10.1371/journal.pone.0022648.Suche in Google Scholar PubMed PubMed Central
Darriba, D., Taboada, G.L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9: 772, https://doi.org/10.1038/nmeth.2109.Suche in Google Scholar PubMed PubMed Central
de Rezende, M.B., Herrera, H.M., Carvalho, C.M.E., Carvalho, E.A.A., Ramos, C.A.N., de Araújo, F.R., Torres, J.M., and de Oliveira, C.E. (2017). Detection of Leishmania spp. in bats from an area of Brazil endemic for visceral Leishmaniasis. Transbound. Emerg. Dis. 64: e36–e42, https://doi.org/10.1111/tbed.12597.Suche in Google Scholar PubMed
Diaz, M.M., Solari, S., Aguirre, L.F., Aguiar, L.M.S., and Barquez, R.M. (2016). Clave de identificación de los murciélagos de Sudamérica. Publicación Especial N° 2. PCMA (Programa de Conservación de los Murciélagos de Argentina).Suche in Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3: 294–299.Suche in Google Scholar
Hall, T. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95–98.Suche in Google Scholar
Hebert, P.D.N., Cywinska, A., Ball, S.L., and DeWaard, J.R. (2003). Biological identifications through DNA barcodes. Proc. Roy. Soc. Lond. B Biol. Sci. 270: 313–321, https://doi.org/10.1098/rspb.2002.2218.Suche in Google Scholar PubMed PubMed Central
Hernández-Dávila, A., Vargas, J.A., Martínez-Méndez, N., Lim, B.K., Engstrom, M.D., and Ortega, J. (2012). DNA barcoding and genetic diversity of phyllostomid bats from the Yucatan Peninsula with comparisons to Central America. Mol. Ecol. Resour. 12: 590–597.10.1111/j.1755-0998.2012.03125.xSuche in Google Scholar PubMed
Hoffmann, F.G. and Baker, R.J. (2003). Comparative phylogeography of short-tailed bats (Carollia: Phyllostomidae). Mol. Ecol. 12: 3403–3414, https://doi.org/10.1046/j.1365-294x.2003.02009.x.Suche in Google Scholar PubMed
Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16: 111–120, https://doi.org/10.1007/bf01731581.Suche in Google Scholar
Kumar, S., Stecher, G., and Tamura, K. (2016). MEGA7 : molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33: 1870–1874, https://doi.org/10.1093/molbev/msw054.Suche in Google Scholar PubMed PubMed Central
Kunz, T.H., Braun, T.E., Bauer, D., Lobova, T., and Fleming, T.H. (2011). Ecosystem services provided by bats. Ann. N. Y. Acad. Sci. 1223: 1–38, https://doi.org/10.1111/j.1749-6632.2011.06004.x.Suche in Google Scholar PubMed
Larsen, P.A., Marchán-Rivadeneira, M.R., and Baker, R.J. (2013). Speciation dynamics of the fruit-eating bats (genus Artibeus): with evidence of ecological divergence in Central American populations. In: Adams, R.A. and Pedersen, S.C. (Eds.). Bat evolution, ecology, and conservation. Springer, New York, pp. 315–339.10.1007/978-1-4614-7397-8_16Suche in Google Scholar
Librado, P. and Rozas, J. (2009). DnaSP v5 : a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452, https://doi.org/10.1093/bioinformatics/btp187.Suche in Google Scholar PubMed
Lim, B.K. and Arcila, L.M. (2016). DNA barcoding of Jamaican bats: implications to Neotropical biodiversity. Mitochondrial DNA 27: 3013–3019.10.3109/19401736.2015.1063047Suche in Google Scholar PubMed
Lopez-Baucells, A., Rocha, R., Bobrowiec, P.E.D., Palmeirim, J.M., and Meyer, C.F.J. (2016). Field guide to Amazonian bats. INPA, Manaus.Suche in Google Scholar
Loureiro, L., Gregorin, R., and Perini, F. (2018a). Diversity, morphological phylogeny, and distribution of bats of the genus Molossus E. Geoffroy, 1805 (Chiroptera, Molossidae) in Brazil. Zoosystema 40: 425–452, https://doi.org/10.5252/zoosystema2018v40a18.Suche in Google Scholar
Loureiro, L., Lim, B.K., and Engstrom, M.D. (2018b). A new species of mastiff bat (Chiroptera, Molossidae, Molossus) from Guyana and Ecuador. Mamm. Biol. 89: 10–21, https://doi.org/10.1016/j.mambio.2018.01.008.Suche in Google Scholar
Mantilla-Meluk, H. (2014). Defining species and species boundaries in Uroderma (Chiroptera: Phyllostomidae) with a description of a new species, 325. Occasional Papers, Museum of Texas Tech University, pp. 1–25.Suche in Google Scholar
Ondrejicka, D.A., Locke, S.A., Morey, K., Borisenko, A.V., and Hanner, R.H. (2014). Status and prospects of DNA barcoding in medically important parasites and vectors. Trends Parasitol. 30: 582–591, https://doi.org/10.1016/j.pt.2014.09.003.Suche in Google Scholar PubMed
Puillandre, N., Brouillet, S., and Achaz, G. (2021). ASAP: assemble species by automatic partitioning. Mol. Ecol. Resour. 21: 609–620, https://doi.org/10.1111/1755-0998.13281.Suche in Google Scholar PubMed
Racero-Casarrubia, J., Ballesteros-Correa, J., and Perez-Torres, J. (2015). Mamíferos del departamento de Córdoba-Colombia: historia y estado de conservación. Biota Colomb. 16: 128–148.Suche in Google Scholar
Ramírez-Chaves, H.E., Suárez-Castro, A.F., and González-Maya, J.F. (2016). Cambios recientes a la lista de los mamíferos de Colombia. Mammal. Notes 3: 1–9, https://doi.org/10.47603/manovol3n1.1-9.Suche in Google Scholar
Rodriguez, I.G. and Loaiza, J.R. (2017). American trypanosomiasis, or Chagas disease, in Panama: a chronological synopsis of ecological and epidemiological research. Parasites Vectors 10: 459, https://doi.org/10.1186/s13071-017-2380-5.Suche in Google Scholar PubMed PubMed Central
Sikes, R. and The Animal Care and Use Committee of the American Society of Mammalogists. (2016). 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J. Mammal. 97: 663–688, https://doi.org/10.1093/jmammal/gyw078.Suche in Google Scholar PubMed PubMed Central
Solari, S. and Martínez-Arias, V. (2014). Cambios recientes en la sistemática y taxonomía de murciélagos Neotropicales (Mammalia: Chiroptera). Therya 5: 167–196.10.12933/therya-14-180Suche in Google Scholar
Vela, I.V. and Pérez, J. (2012). Murciélagos asociados a remanentes de bosque seco tropical en un sistema de ganadería extensiva (Colombia). Chiropt. Neotrop. 18: 1089–1100.Suche in Google Scholar
Zurc, D. and Velasco, P.M. (2010). Análisis morfológico y morfométrico de Carollia colombiana Cuartas et al. 2001 y C. monohernandezi Muñoz et al. 2004 (Phyllostomidae: Carollinae) en Colombia. Chiropt. Neotrop. 16: 549–567.Suche in Google Scholar
Supplementary Material
The online version of this article offers supplementary material (https://doi.org/10.1515/mammalia-2020-0138).
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Artikel in diesem Heft
- Frontmatter
- Conservation
- Ansorge’s cusimanse in Angola: 100 years apart, new records contribute to the species known range
- Abundance of the exploited red-rumped agouti (Dasyprocta leporina Rodentia: Dasyproctidae) on the island of Trinidad
- Biogeography
- The roles of possible geographic barriers and geological events on the phylogeographic structure of the Eastern broad toothed field mouse (Apodemus mystacinus)
- First record of Blanford’s Fox Vulpes cana (Blanford, 1877) from Iraq
- New records and southern range extension of the Annamite striped rabbit Nesolagus timminsi in Vietnam
- Ecology
- A pilot study of the use of dry dog food as an alternative attractant in mesocarnivore studies
- Seasonal diet composition of Himalayan goral (Naemorhedus goral) in Kajinag National Park, Jammu and Kashmir, India
- Seasonal and daily activity patterns of mammals in the colony of great cormorants
- First North African record of a melanistic common genet (Genetta genetta Linnaeus, 1758)
- Albinism in Brazilian common opossums (Didelphis aurita)
- Evolutionary biology
- Brain size evolution in small mammals: test of the expensive tissue hypothesis
- Taxonomy/phylogeny
- DNA barcoding of bats (Chiroptera) from the Colombian northern region
- Morphology and genetics concur that Anoura carishina is a synonym of Anoura latidens (Chiroptera, Glossophaginae)
- Taxonomy of Ctenomys (Rodentia: Ctenomyidae) in northwestern Patagonia, Argentina: the occurrence of the “mendocinus” lineage