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Type: Article
Published: 2022-09-21
Page range: 430-452
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Systematic review of Myotis (Chiroptera, Vespertilionidae) from Chile based on molecular, morphological, and bioacoustic data

Fundação Oswaldo Cruz, Fiocruz Mata Atlântica, 22713-375, Rio de Janeiro, RJ, Brazil
Universidad Santo Tomás, Centro de Investigación e Innovación Para el Cambio Climático, 8370003, Santiago, Chile 3Bioecos E.I.R.L., Las Condes, Santiago, Chile. Programa para la Conservación de los Murciélagos de Chile, Santiago, Chile
Universidad Bernardo O’Higgins, Centro de Investigación en Recursos Naturales y Sustentabilidad, Santiago, Chile
Bioecos E.I.R.L., Las Condes, Santiago, Chile
Smithsonian Institution, National Museum of Natural History, 20560, Washington, DC, USA
Fundação Oswaldo Cruz, Fiocruz Mata Atlântica, 22713-375, Rio de Janeiro, RJ, Brazil
Mammalia Echolocation calls mitochondrial gene multivariate analysis Myotinae Myotis arescens phylogenetics South America

Abstract

Myotis is the most diverse genus of bats in the world, with more than 30 species recognized in the Neotropics. However, many of these species represent cryptic complexes and are evidence of the existence of hidden diversity in several regions. Using an integrative approach based on molecular, morphological, and bioacoustic data, we performed a systematic review of Myotis species from Chile. Phylogenetic inference using cytochrome-b indicated the existence of three monophyletic lineages, and qualitative and quantitative morphological analyses supported these lineages as distinct and morphologically diagnosable taxa. Analysis of discriminant functions using parameters of echolocation calls also indicates the existence of three distinct bioacoustic clusters. Thus, all lines of evidence congruently indicate the existence of three distinct taxa. As a result, we recognize Myotis arescens as a valid and distinct species and define its taxonomic limits from the other species from Chile, Myotis atacamensis and Myotis chiloensis.

 

References

  1. Brunet-Rossini, A.K. & Wilkinson, G.S. (2009) Methods for age estimation and study of senescence in bats. In: Kunz, T.H. & Parsons, S. (Eds.), Ecological and behavioral methods for the study of bats. The Johns Hopkins University Press, Baltimore, pp. 315–325.
    Caraballo, D.A., Montani, M.E., Martýnez, L.M., Antoniazzi, L.R., Sambrana, T.C., Fernandez, C., Cisterna, D.M., Beltrán, F.J. & Colombo, V.C. (2020) Heterogeneous taxonomic resolution of cytochrome b gene identification of bats from Argentina: implications for field studies. PLoS One, 15, e0244750. https://doi.org/10.1371/journal. pone.0244750
    Carrión-Bonilla, C.A. & Cook, J.A. (2020) A new bat species of the genus Myotis with comments on the phylogenetic placement of M. keaysi and M. pilosatibialis. Therya, 11, 508–532. https://doi.org/10.12933/therya-20-999 ISSN 2007-3364
    Chornelia, A., Lu, J. & Hughes, A.C. (2022) How to accurately delineate morphologically conserved taxa and diagnose their phenotypic disparities: species delimitation in cryptic Rhinolophidae (Chiroptera). Frontiers in Ecology and Evolution, 10, a854509. https://doi.org/10.3389/fevo.2022.854509
    Darriba, D., Taboada G. L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, a772. https://doi.org/10.1038/nmeth.2109
    Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797. https://doi.org/10.1093/nar/gkh340
    Hasegawa, M., Kishino, H. & Yano, T. (1985) Dating of human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution, 22, 160–174. https://doi.org/10.1007/BF02101694
    Heller, K.G. & von Helversen, O. (1989) Resource partitioning of sonar frequency bands in rhinolophoid bats. Oecologia, 80, 178–186. https://doi.org/10.1007/bf00380148
    Honaker, J., King, G. & Blackwell, M. (2011) Amelia II: A program for missing data. Journal of Statistical Software, 45, 1–47. https://doi.org/10.18637/jss.v045.i07
    Huelsenbeck, J.P., Ronquist, F., Nielsen, R. & Bollback, J.P. (2001) Bayesian Inference of phylogeny and its impact on evolutionary biology. Science, 294, 2310–2314. https://doi.org/10.1126/science.1065889
    Jones, G. & Holderied, M.W. (2007) Bat echolocation calls: adaptation and convergent evolution. Proceedings of the Royal Society B, 247, 905–912. https://doi.org/10.1098/rspb.2006.0200
    Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. & Drummond, A. (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649. https://doi.org/10.1093/bioin forma tics/bts199
    Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111−120. https://doi.org/10.1007/BF01731581
    Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamuda, K. (2018) MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Molecular Biology and Evolution, 35, 1547−1549. https://doi.org/10.1093/molbev/msy096
    Larsen, R.J., Knapp, M.C., Genoways, H.H., Khan, F.A.A., Larsen, P.A., Wilson, D.E. & Baker, R.J. (2012a) Genetic diversity of Neotropical Myotis (Chiroptera: Vespertilionidae) with an emphasis on South American species. PLoS One, 7, e46578. https://doi.org/10.1371/journal.pone.0046578
    Larsen, R.J., Larsen, P.A., Genoways, H.H., Catzeflis, F.M., Geluso, K., Kwiecinski, K.K., Pedersen, S.C., Simal, F. & Baker, R.J. (2012b) Evolutionary history of Caribbean species of Myotis, with evidence of a third Lesser Antillean endemic. Mammalian Biology, 77, 124–134. https://doi.org/10.1016/j.mambio.2011.11.003
    LaVal, R.K. (1973) A revision of the Neotropical bats of the genus Myotis. Natural History Museum of Los Angeles County, Science Bulletin, 15, 1−54.
    Lilley, T.M., Sävilammi, T., Ossa, G., Blomberg, A.S., Vasemägi, A., Yung, V., Vendrami, D.L.J. & Johnson, J.S. (2020) Population connectivity predicts vulnerability to white-nose syndrome in the Chilean Myotis (Myotis chiloensis)—A genomics approach. G3: Genes, Genomes, Genetics, 10, 2117–212. https://doi.org/10.1534/g3.119.401009
    Martins, F.M., Ditchfield, A.D., Meyer, D. & Morgante, J.S. (2007) Mitochondrial DNA phylogeography reveals marked population structure in the common vampire bat, Desmodus rotundus (Phyllostomidae). Journal of Zoological Systematic and Evolutionary Research, 45, 372–378. https://doi.org/10.1111/j.1439-0469.2007.00419.x
    MDD (2022) Mammal Diversity Database. Version 1.8. Zenodo. Available from: https://zenodo.org/record/4139818#.YxVNb3ZbyUk (accessed 5 Septebmer 2022) http://doi.org/10.5281/zenodo.4139818
    Moratelli, R. & Oliveira, J.A. (2011) Morphometric and morphological variation in South American populations of Myotis albescens (Chiroptera: Vespertilionidae). Zoologia, 28, 789–802. https://doi.org/10.1590/S1984-46702011000600013
    Moratelli, R. & Wilson, D.E. (2011) A new species of Myotis Kaup, 1829 (Chiroptera, Vespertilionidae) from Ecuador. Mammalian Biology, 76, 608−614. https://doi.org/10.1016/j.mambio.2010.10.003
    Moratelli, R. & Wilson, D.E. (2014) A new species of Myotis (Chiroptera, Vespertilionidae) from Bolivia. Journal of Mammalogy, 95, 17−25. https://doi.org/10.1644/14-MAMM-149
    Moratelli, R., Peracchi, A.L., Dias, D. & Oliveira, J.A. (2011) Geographic variation in South American populations of Myotis nigricans (Schinz, 1821) (Chiroptera, Vespertilionidae), with the description of two new species. Mammalian Biology, 76, 592−607. https://doi.org/10.1016/j.mambio.2011.01.003
    Moratelli, R., Gardner, A.L., Oliveira, J.A. & Wilson, D.E. (2013) Review of Myotis (Chiroptera, Vespertilionidae) from northern South America, including description of a new species. American Museum Novitates, 3780, 1−36. https://doi.org/10.1206/3780.2
    Moratelli, R., Wilson, D.E., Gardner, A.L., Fisher, R.D. & Gutiérrez, E.E. (2016) A new species of Myotis (Chiroptera, Vespertilionidae) from Suriname. Special Publications of the Museum of Texas Tech University, 65, 49–66.
    Moratelli, R., Wilson, D.E., Novaes, R.L.M., Helgen, K.M. & Gutiérrez, E.E. (2017) Caribbean Myotis (Chiroptera, Vespertilionidae), with description of a new species. Journal of Mammalogy, 98, 994–1008. https://doi.org/10.1093/jmammal/gyx062
    Moratelli, R., Burgin, C., Cláudio, V.C., Novaes, R.L.M., López-Baucells, A. & Haslauer, R. (2019a) Family Vespertilionidae (Vesper Bats). In: Wilson, D.E. & Mittermeier, A.R. (eds.), Handbook of the mammals of the world. Vol. 9. Bats. Lynx Editions, Barcelona, pp. 716–981.
    Moratelli, R., Novaes, R.L.M., Carrión-Bonilla, C. & Wilson, D.E. (2019b) A new species of Myotis (Chiroptera, Vespertilionidae) from Peru. Special Publications of the Museum of Texas Tech University, 71, 239–256.
    Novaes, R.L.M. (2019) Chilean Myotis, Myotis chiloensis. In: Wilson, D.E. & Mittermeier, A.R. (Eds.), Handbook of the mammals of the world. Vol. 9. Bats. Lynx Editions, Barcelona, pp. 939–940.
    Novaes, R.L.M., Wilson, D.E., Ruedi, M. & Moratelli, R. (2018) The taxonomic status of Myotis aelleni Baud, 1979 (Chiroptera, Vespertilionidae). Zootaxa, 4446 (2), 257–264. https://doi.org/10.11646/zootaxa.4446.2.5
    Novaes, R.L.M., Cláudio, V.C., Larsen, R.J., Wilson, D.E., Weksler, M. & Moratelli, R. (2021a) The taxonomic status of Myotis nesopolus larensis (Chiroptera, Vespertilionidae) and new insights on the diversity of Caribbean Myotis. ZooKeys, 1015, 145–167. https://doi.org/10.3897/zookeys.1015.59248
    Novaes, R.L.M, Cláudio, V.C., Carrión-Bonilla, C., Abreu, E.F., Wilson, D.E., Maldonado, J.E. & Weksler, M. (2021b [2022]) Variation in the Myotis keaysi complex (Chiroptera, Vespertilionidae), with description of a new species from Ecuador. Journal of Mammalogy, 103, 540–559. https://doi.org/10.1093/jmammal/gyab139
    Novaes, R.L.M., Wilson, D.E. & Moratelli, R. (2021c) A new species of Myotis (Chiroptera, Vespertilionidae) from Uruguay. Vertebrate Zoology, 71, 711–722. https://doi.org/10.3897/vz.71.e73146
    Novaes, R.L.M., Wilson, D.E. & Moratelli, R. (2022) Catalogue of primary types of Neotropical Myotis (Chiroptera, Vespertilionidae). ZooKeys, 1105, 127–164. https://doi.org/10.3897/zookeys.1105.85055
    Novaes, R.L.M., LaVal, R.K., Wilson, D.E. & Moratelli, R. (2022b) Redescription of Myotis atacamensis (Chiroptera: Vespertilionidae) with neotype designation. Zoologia, 39, e21026. https://doi.org/10.1590/S1984-4689.v39.e21026
    Osgood, W.H. (1943) The mammals of Chile. Field Museum of Natural History, Zoological Series, 30, 1–268. https://doi.org/10.5962/bhl.title.3842
    Ossa, G. & Rodríguez-San Pedro, A. (2015) Myotis chiloensis (Chiroptera: Vespertilionidae). Mammalian Species, 47 (922), 51–56. https://doi.org/10.1093/mspecies/sev005
    Padial, J.M., Miralles, A., La Riva, I.D. & Vences, M. (2010) The integrative future of taxonomy. Frontiers in Zoology, 7, e16. https://doi.org/10.1186/1742-9994-7-16
    Patterson, B.D., Webala, P.W., Peterhans, J.C.K., Goodman, S.M., Bartonjo, M. & Demos, T.C. (2019) Genetic variation and relationships among Afrotropical species of Myotis (Chiroptera: Vespertilionidae). Journal of Mammalogy, 100, 1130–1143. https://doi.org/10.1093/jmammal/gyz087
    Pavan, A.C., Bobrowiec, P.E.D. & Percequillo, A.R. (2018) Geographic variation in a South American clade of mormoopid bats, Pteronotus (Phyllotia), with description of a new species. Journal of Mammalogy, 99 (3), 624–645. https://doi.org/10.1093/jmammal/gyy048
    Rambaut, A. & Drummond, A.J. (2009) Tracer Version 1.5. MCMC Trace Analysis Packpage. Available from: http://tree.bio.ed.ac.uk/software/tracer/ (accessed 8 May 2017)
    Ridgway, R. (1912) Color standards and color nomenclature. Privately published, Washington, D.C., iii + 43 pp., LIII pp.
    Rodríguez-San Pedro, A., Allendes, J.L., Castillo, M.L., Peñaranda, D. & Peña-Gómez, F.T. (2014) Distribution extension and new record of Myotis atacamensis (Lataste, 1892) (Chiroptera: Vespertilionidae) in Chile. Check List, 10, 1164–1166. https://doi.org/10.15560/10.5.1164
    Rodríguez-San Pedro, A., Peñaranda, D.A., Allendes, J.L. & Castillo, M.L. (2015) Update on the distribution of Myotis atacamensis (Chiroptera: Vespertilionidae): southernmost record and description of its echolocation calls. Chiroptera Neotropical, 21, 1342–1346.
    Rodríguez-San Pedro, A., Allendes, J.L., Beltrán, C., Mayorga, M. & Mella-Ávila, J. (2020) Additions to the ecology, distribution, and natural history of the endangered bat Myotis atacamensis (Lataste, 1892) (Chiroptera: Vespertilionidae) in Chile. Studies on Neotropical Fauna and Environment, 56, 146–152. https://doi.org/10.1080/01650521.2020.1770452
    Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574. https://doi.org/10.1093/bioinformatics/btg180
    Ruedi, M. & Mayer, F. (2001) Molecular systematics of bats of the genus Myotis (Vespertilionidae) suggests deterministic ecomorphological convergences. Molecular Phylogenetics and Evolution, 21, 463−448. https://doi.org/10.1006/mpev.2001.1017
    Ruedi, M., Csorba, G., Lin, L.K. & Chou, C.H. (2015) Molecular phylogeny and morphological revision of Myotis bats (Chiroptera: Vespertilionidae) from Taiwan and adjacent China. Zootaxa, 3920 (2), 301–342. https://doi.org/10.11646/zootaxa.3920.2.6
    Sarkar, D. (2008) Lattice: multivariate data visualization with R. Springer-Verlag, New York, New York, XVIII + 268 pp.
    Sedlock, J.L., Heaney, L.R., Balete, D.S. & Ruedi, M. (2020) Philippine bats of the genus Kerivoula (Chiroptera: Vespertilionidae): overview and assessment of variation in K. pellucida and K. whiteheadi. Zootaxa, 4755 (3), 454–490. https://doi.org/10.11646/zootaxa.4755.3.2
    Schuller, G. & Moss, C.F. (2004) Introduction: vocal control and acoustically guided behavior in bats. In: Thomas, J.A., Moss, C.F. & Vater, M. (Eds.), Echolocation in bats and dolphins. The Chicago University Press, Chicago, Illinois, pp. 3–16.
    Stadelmann, B., Lin, L.K., Kunz, T.H. & Ruedi, M. (2007) Molecular phylogeny of New World Myotis (Chiroptera, Vespertilionidae) inferred from mitochondrial and nuclear DNA genes. Molecular Phylogenetics and Evolution, 43, 32–48. https://doi.org/10.1016/j.ympev.2006.06.019
    Tabachnick, B.G. & Fidell, L.S. (2014) Multivariate Analysis of Variance (MANOVA). In: Lovric, M. (Wd.), International Encyclopedia of Statistical Science. Springer, Berlin, Heidelberg, pp. 902–904.
    Venables, W.N. & Ripley, B.D. (2002) Modern applied statistics with R. Springer-Verlag, New York, New York, XII + 498 pp.
    Wheeler, Q.D. (1999) Why the phylogenetic species concept?—Elementary. Journal of Nematology, 31, 134–141.
    Wickham, H., François, R., Henry, L. & Müller, K. (2017) Package ‘dplyr’. R Foundation for Statistical Computing, Vienna. Available from: https://cran.r-project.org/web/packages/dplyr/index.html (accessed 5 September 2022)
    Wilson, D.E. (2007 [2008]) Genus Myotis. In: Gardner, A.L. (Ed.), Mammals of South America - marsupials, xenarthrans, shrews and bats. University of Chicago Press, Chicago, Illinois and London, pp. 468–480.
    Zachos, F.E. (2016) Species concepts in biology: historical development, theoretical foundations and practical relevance. Springer International Publishing, Cham, XII + 220 pp.

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