A new bat species of the genus Myotis with comments on the phylogenetic placement of M. keaysi and M. pilosatibialis
Keywords:
Armien’s Myotis, Chiriquí province, Cordillera Oriental, cryptic diversity, Myotis armiensis, Neotropics, Valle del Silencio.Abstract
Molecular studies of Neotropical Myotis (Chiroptera, Vespertilionidae) in the last decade have uncovered substantial cryptic diversity. One example is M. keaysi pilosatibialis, which is characterized by a complex taxonomy derived from low morphological variation. Herein, we studied cryptic diversity of a high elevation clade from premontane and montane forest of Chiriquí Province (Panamá), Cordillera Oriental (Ecuador), and Valle del Silencio (Costa Rica). Additionally, we disentangle relationships of M. k. keaysi and M. k. pilosatibialis by determining their phylogenetic placement within the Neotropical Myotis radiation. In the process, we identified a new lineage of species level hierarchy that is described herein. We used an integrative taxonomy approach, using a combination of linear morphometrics, qualitative morphology, molecular phylogenetics, and climatic analysis. The newly identified lineage is a sister species to M. pilosatibialis str., but differs from M. sp. (Quintana Roo, México), M. keaysi str., and M. oxyotus gardneri in size and other quantitative morphological characters in addition to both nuclear and mitochondrial DNA sequence divergence. Based on our phylogenetic analysis of partial cytochrome b sequence, the polyphyly of M. keaysi str. and M. pilosatibialis str. is resolved, with M. keaysi str. paraphyletic to M. ruber and M. simus. Myotis pilosatibialis is part of a monophyletic clade that is sister to the newly identified species. This report refines our understanding of taxonomy and systematics of the Myotis pilosatibialis complex of bats, identifies and describes a new species of Myotis, and more broadly it contributes to efforts to characterize species in this genus in Neotropical environments. Based on its distribution, we classified this newly described species as paramontane due to its restriction to premontane and montane forest of Chiriquí Province (Panamá), Valle del Silencio (Costa Rica), and Cordillera Oriental (Ecuador). These habitats are susceptible to the effects of climate change, in addition to ongoing habitat destruction.References
BAUD, F. J., AND H. MENU. 1993. Paraguayan bats of the genus Myotis, with a redefinition of Myotis simus (Thomas, 1901). Revue Suisse de Zoologie 100:595-607.
BAIRD, A. B., D. M. HILLIS, J. C. PATTON, AND J. W. BICKHAM. 2008. Evolutionary history of the genus Rhogeessa (Chiroptera: Vespertilionidae) as revealed by mitochondrial DNA sequences. Journal of Mammalogy 89:744-754.
BECK, M. W. 2017. ggord: Ordination Plots with ggplot2. R Package version 1.0.0.
BOUCKAERT, R., T. G.VAUGHAN, J. BARIDO-SOTTANI, S. DUCHÊNE, M. FOURMENT, A. GAVRYUSHKINA, J. HELED, G. JONES, D. KÜHNERT, N. DE MAIO, M. MATSCHINER, F. K MENDES, N. F. MÜLLER, H. A, OGILVIE, L. DU PLESSIS, A. POPINGA, A. RAMBAU, D. RASMUSSEN, I. SIVERONI, M. A. SUCHARD, C-H. WU, D. XIE, C. ZHANG, T. STADLER, AND A. J. DRUMMONDS. 2019. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. Plos Computational Biology 15:1-28.
BICKFORD, D., D. J. LOHMAN, NAVJOT. S. S, P. K. L, NG , R. MEIER, K. WINKER, K. K. INGRAM, AND I. DAS. 2007. Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution 22:148-155.
CARØE, C., S. GOPALAKRISHNAN, L. VINNER, S. S. T. MAK, M. H. S. SINDING, J. A. SAMANIEGO, N. WALES, T. SICHERITZ-PONTEN, AND M. T. P. GILBERT. 2018. Single-tube library preparation for degraded DNA, Methods in Ecology and Evolution 9:410-419.
CHAVERRI, G., I. GARIN, A. ALBERDI, L. JIMENEZ, C. CASTILLO-SALAZAR, AND J. AIHARTZA. 2016. Unveiling the hidden bat diversity of a neotropical montane forest. Plos one, 11:e0162712.
CLARE, E. L., B. K. LIM, M. B. FENTON, AND P. D. N. HEBERT. 2011. Neotropical Bats: Estimating Species Diversity with DNA Barcodes. Plos One 6:1-14.
DE QUEIROZ, K. 2007. Species Concepts and Species Delimitation. Systematic Biology 56:879 - 886.
DIERCKXSENS, N., P. MARDULYN, AND G. SMITS. 2016. NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Research 45:1-9.
DUNNUM, J. L., B. S, MCLEAN, R. C. DOWLER, AND THE SYSTEMATIC COLLECTIONS COMMITTEE OF THE AMERICAN SOCIETY OF MAMMALOGIST. 2018. Mammal collections of the Western Hemisphere: a survey and directory of collections. Journal of Mammalogy 99:1307-1322.
EDGAR, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32:1792-1797.
EICK, G. N., D. S. JACOBS, AND C. A. MATTHEE. 2005. A nuclear DNA phylogenetic perspective on the evolution of echolocation and historical biogeography of extant bats (Chiroptera). Molecular Biology and Evolution 22:1869-1886.
FICK, S. E., AND R. J, HIJMANS. 2017. WorldClim2: new 1km spatial resolution climate surface for global land areas. International Journal of Climatology 37:4302-4315.
FLORIO, A. M., C. M. INGRAM, H. A. RAKOTONDRANOVY, E. E. LOUIS, C. J. RAXWORTHY. 2012. Detecting cryptic speciation in the widespread and morphologically conservative carpet chamelon (Furcifer lateralis) of Madagascar. Journal of Evolutionary Biology 25:1399-1414.
FLOT, J. F. 2010. SEQPHASE: a web tool for interconverting phase input/output files and fasta sequence alignments. Molecular Ecology Resources 10:162-166.
FOX, J., AND S. WEISBERG. 2019. An R Companion to Applied Regression. Third edition. Sage, Thousands Oaks CA.
GALBREATH, K. E., E. P. HOBERG, J. A. COOK, B. ARMIÉN, K. C. BELL, M. L. CAMPBELL, J. DUNNUM, A. T. DURSAHINHAN, R. P. ECKERLIN, S. L. GARDNER, S. E. GREIMAN, H. HENTTONEN, F. A. JIMÉNEZ, A. VA. KOEHLER, B. NYAMSUREN, V. V. TKACH, F.TORRES-PÉREZ, A.TSVETKOVA ,AND A. HOPE. 2019. Building an integrated infrastructure for exploring biodiversity: field collections and archives of mammals and parasites. Journal of Mammalogy 100:382-393.
HAYNIE, M. L., J. G. BRANT, L. R. MCALILEY, J. P. CARRERA, M. A, REVELEZ, D. A, PARISH, X. VITERI, C. JONES, AND C. J. PHILLIPS. 2006. Investigations in a Natural Corridor between two national parks in Central Ecuador: Results from the Sowell Expedition, 2001. Occasional Papers, Museum of Texas Tech University 263:1-16.
HELED, J., AND A. J. DRUMMOND. 2010. Bayesian Inference of Species Trees from Multilocus Data. Molecular Biology and Evolution 27:570-580.
HERNANDEZ-MEZA, B., Y. DOMINGUEZ-CASTELLANOS, AND J. ORTEGA. 2005. Myotis keaysi. Mammalian Species 785:1-3.
HOFFMANN, F. G., AND R. J. BAKER. 2001. Systematics of bats of the genus Glossophaga (Chiroptera: Phyllostomidae) and phylogeography in G. soricina based on the cytochrome-b gene. Journal of Mammalogy 82:1092-1101.
HONAKER, J., G. KING, AND M. BLACKWELL. 2011. Amelia II: A Program for Missing Data. Journal of Statistical Software 45:1-47.
JONES, G. 2017. Algorithmic improvements to species delimitation and phylogeny estimation under the multispecies coalescent. Journal of Mathematica Biology 74:447–467.
JONES, G. speciesDA.jar. htpp://indriid.com/2014/speciesDA.jar. Accessed 15 July 2020.
KALYAANAMOORTHY, S., B. Q. MINH, T. K. F. WONG, A. VON HAESELER, AND L. S. JERMIIN. 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14:587-591.
KASSAMBARA, A. 2020. Rstatix: Pipe-Friendly Framework for Basic Statistical Test. R package version 0.6.0.
KASSAMBARA, A., AND F. MUNDT. 2020. factoextra: Extract and Visualize the Results of Multivariate Data Analyses. R package version 1.0.7.999.
KAWAI, K., N. KONDO, N. SASAKI, D. FUKUI, H. DEWA, M. SATO, AND Y.YAMAGAI. 2006. Distinguishing between cryptic species Myotis ikonnikovi and M. brandtii gracilis in Hokkaido, Japan: Evaluation of a novel diagnostic morphological feature using molecular methods. Acta Chiropterologica 8:95-102.
KAWAI, K., M. NIKAIDO, HARADA, S. MATSUMURA, L-K, LIN, Y.WU, M. HASEGAWA, AND N. OKADA. 2003. The status of the Japanese and East Asian bats of the genus Myotis (Vespertillonidae) based on mitochondrial sequences. Molecular Phylogenetics and Evolution 28:297-307.
KOOPMAN, K. F. 1983. Two general problems involved in systematics and zoogeography of bats. Pp. 412-415 in Advances in herpetology and evolutionary biology. Essays in honor of Ernest E Williams (Rhodin, G. J., and K. Miyata, eds). Museum of Comparative Zoology, Cambridge, Massachusetts, EE.UU.
KUMAR, S., G. STECHER, AND K. TAMURA. 2016. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution 33:1870-1874.
LA VAL, R. K. 1973. A revision of Neotropical bats of the genus Myotis. Natural History Museum of Los Angeles County. Science Bulletin:1-54.
LACK, J. B., Z. P. ROEHRS, C. E. STANLEY, M. RUEDI, AND R. A. VAN DEN BUSSCHE. 2010. Molecular phylogenetics of Myotis indicate familial-level divergence for the genus Cistugo (Chiroptera). Journal of Mammalogy 91:976-992.
LARSEN, R. J., M. C. KNAPP, H. H. GENOWAYS, F. A ANWARALI KHAN, P. LARSEN, D.WILSON, AND R. J. BAKER. 2012a. Genetic Diversity of Neotropical Myotis (Chiroptera: Vespertilionidae) with an Emphasis on South American Species. Plos One 7:1-9.
LARSEN, R. J., P. LARSEN, H. H. GENOWAYS, F. M. CATZEFLIS, K. GELUSOS, G.G KWIECINSKI, S. C. PEDERSEN, F. SIMAL, AND R. J. BAKER. 2012b. Evolutionary history of Caribbean species of Myotis, with evidence of a third Lesser Antillean endemic. Mammalian Biology 77:124-134.
LINDGREEN, S. 2012. AdapterRemoval: easy cleaning of next-generation sequencing reads. BMC Research Notes 5:337-337.
LÓPEZ -GONZÁLEZ, C., S. J. PRESLEY, R. D. OWEN, M.R. WILLIG. 2001. Taxonomic status of Myotis (Chiroptera: Vespertilionidae) in Paraguay. Journal of Mammalogy 82:138-160.
MAK, S. S. T., S. GOPALAKRISHNAN, C. CARØE, C. GENG, S. LIU, M. H. S. SINDING, L. F. K. KUDERNA, W. ZHANG, S. FU, F. G. VIEIRA, M. GERMONPRE, H. BOCHERENS, S. FEDOROV, B. PETERSEN, T. SICHERITZ-PONTEN, T. MARQUES-BONET, G. ZHANG, H. JIANG, AND M.T.P. GILBERT. 2017. Comparative performance of the BGISEQ-500 vs Illumina HiSeq2500 sequencing platforms for palaeogenomic sequencing. Gigascience 6:1-13.
MAMMAL DIVERSITY DATABASE. 2020. www.mammal.diversity.org. American Society of Mammalogist. Accessed 2020-04-19.
MANTILLA-MELUK, H., AND J. MUNOZ-GARAY. 2014. Biogeography and taxonomic status of Myotis keaysi pilosatibialis LaVal 1973 (Chiroptera: Vespertilionidae). Zootaxa 3793:60-70.
MATTHEE, C. A., AND S. K. DAVIS. 2001. Molecular insights into the evolution of the family Bovidae: A nuclear DNA perspective. Molecular Biology and Evolution 18:1220-1230.
MCLEAN, B. S., D. J, JACKSON, AND J. A. COOK. 2016. Rapid divergence and gene flow at high latitudes shape the history of Holarctic ground squirrels (Urocitellus). Molecular Phylogenetics and Evolution 102:174-188.
MENG, G., Y. LI, C. YANG, AND S. LIU. 2019 MitoZ: a toolkit for animal mitochondrial genome assembly, annotation and visualization. Nucleic Acids Research 47:1-7.
MORATELLI, R., AND WILSON, D. 2011. A new species of Myotis Kaup, 1829 (Chiroptera: Vespertilionidae) from Ecuador. Mammalian Biology 76:608-614.
MORATELLI, R., A. L. GARDNER, J. A. DE OLIVEIRA, AND D. E. WILSON. 2013. Review of Myotis (Chiroptera, Vespertilionidae) from northern South America, including description of a new species. American Museum Novitates:1-36.
MORATELLI, R., AND D. E. WILSON. 2014. A new species of Myotis (Chiroptera, Vespertilionidae) from Bolivia. Journal of Mammalogy 95:17-25.
MORATELLI, R., D. E. WILSON, A. L. GARDNER, R. D. FISHER, AND E. E. GUTIERREZ. 2016. A New Species of Myotis (Chiroptera: Vespertilionidae) from Suriname. Pp 49-66 in Contributions in Natural History: A memorial Volume in Honor of Clyde Jones (Manning, R, Goetze, J.R and Yancey II, F.D). Special Publications Nº 65, Museum of Texas Tech University, Lubbock, EE.UU.
MORATELLI, R., D. E. WILSON, R. L. M. NOVAES, K. M. HELGEN, AND E. E. GUTIERREZ. 2017. Caribbean Myotis (Chiroptera, Vespertilionidae), with description of a new species from Trinidad and Tobago. Journal of Mammalogy 98:994-1008.
MORRONE, J. J. 2017. Neotropical Biogeography: Regionalization and Evolution. CRC Press Taylor & Francis Group, Boca Raton, FL, EE.UU.
NAIDU, A., R. R. FITAK, A. MUNGUIA-VEGA, AND M. CULVER. 2012. Novel primers for complete mitochondrial cytochrome b gene sequencing in mammals. Molecular Ecology Resources 12:191-196.
NGUYEN, L. T., H. A. SCHMIDT, A. VON HAESELER, AND B. Q. MINH. 2015. IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies. Molecular Biology and Evolution 32:268-274.
PATTERSON, B. D., P. W. WEBALA, J. C. K. PETERHANS, S. M. GOODMAN, M. BARTONJO, AND T. C. DEMOS. 2019. Genetic variation and relationships among Afrotropical species of Myotis (Chiroptera: Vespertilionidae). Journal of Mammalogy 100:1130-1143.
QUEIROZ DE, K. 2007. Species Concepts and Species Delimitation. Systematic Biology 56:879-886.
R CORE TEAM. 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna , Austria. URL http://www.R-project.org/.
RAMBAUT, A., A. J. DRUMMOND, D. XIE, G. BAELE, AND M. A. SUCHARD. 2018. Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7. Systematic Biology 67:901-904.
REVELLE, W. 2020. Psych: Procedures for Psychological, Psychometric, and Personality Research. Northwestern University, Evanston, Illinois. R package version 2.0.7.
RIDGWAY, R. 1912. Color standards and color nomenclature. Available at Biodiversity Heritage Library (www.biodiversitylibrary.org).
RICE, W. R. 1989. Analyzing tables of statistical test. Evolution 43:223-225. 01-904.
RODRIGUEZ, R. M., AND L. K. AMMERMAN. 2004. Mitochondrial DNA divergence does not reflect morphological difference between Myotis californicus and Myotis ciliolabrum. Journal of Mammalogy 85:842-851.
ROEHRS, Z. P., J. B. LACK, AND R. A. VAN DEN BUSSCHE. 2010. Tribal phylogenetic relationships within Vespertilioninae (Chiroptera: Vespertilionidae) based on mitochondrial and nuclear sequence data. Journal of Mammalogy 91:1073-1092.
RONQUIST, F., M. TESLENKO, P.VAN DER MARK, D.L, AYRES, A. DARLING, S. HÖHNA, B. LARGET, L. LIU, M. A, SUCHARD, AND J. HUELSENBECK. 2012. MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space. Systematic Biology 61:539-542.
RUEDI, M., AND F. MAYER. 2001. Molecular systematics of bats of the genus Myotis (vespertilionidae) suggests deterministic ecomorphological convergences. Molecular Phylogenetics and Evolution 21:436-448.
RUEDI, M., B. STADELMANN, Y. GAGER, E. J. P. DOUREZY, C. M. FRANCIS, L-K. LIN, A. GUILLÉN-SERVENT, AND A. CIBOIS . 2013. Molecular phylogenetic reconstructions identify East Asia as the cradle for the evolution of the cosmopolitan genus Myotis (Mammalia, Chiroptera). Molecular Phylogenetics and Evolution 69:437-449.
SALICINI, I., C. IBANEZ, AND J. JUSTE. 2011. Multilocus phylogeny and species delimitation within the Natterer’s bat species complex in the Western Palearctic. Molecular Phylogenetics and Evolution 61:888-898.
SCHUBERT, M., S. LINDGREEN, AND L. ORLANDO. 2016. AdapterRemoval v2: rapid adapter trimming, identification, and read merging. BMC Research Notes 9:88-88.
SIKES, R. S., AND M. ANIM CARE USE COMM AMER SOC. 2016. Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. Journal of Mammalogy 97:663-688.
SWOFFORD, D. L. (2003). PAUP*. Phylogentic analysis using parsimony (* and other methods). Version 4.0a168. Sinauer Associates, Sunderland.
STADELMANN, B., L. G. HERRERA, J. ARROYO-CABRALES, J. J. FLORES-MARTINEZ, B. P. MAY, AND M. RUEDI. 2004. Molecular systematics of the fishing bat Myotis (Pizonyx) vivesi. Journal of Mammalogy 85:133-139.
STADELMANN, B., L. K. LIN, T. H. KUNZ, AND M. RUEDI. 2007. Molecular phylogeny of New World Myotis (Chiroptera, Vespertilionidae) inferred from mitochondrial and nuclear DNA genes. Molecular Phylogenetics and Evolution 43:32-48.
STEPHENS, M., N. J. SMITH, AND P. DONNELLY. 2001. A new statistical method for haplotype reconstruction from population data. American Journal of Human Genetics 68:978-989.
TRIFINOPOULOS, J., L. T. NGUYEN, A. VON HAESELER, AND B. Q. MINH. 2016. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research 44:232-235.
VENABLES, W. N., AND RIPLEY, B. D. 2002. Modern Applied Statistics with S. Springer, New York, EE.UU.
VALENCIA, R., C. CERÓN, W. PALACIOS, AND R. SIERRA. 1999. Las formaciones naturales de la Sierra del Ecuador. Pp. 79-108 in Propuesta Clasificación de Vegetación para el Ecuador Contiental (Sierra, R., eds.). Quito, Ecuador: Proyecto INEFAN/GEF-BIRF and EcoCiencia.
VOSS, R. S., B. K. LIM, J. F. DIAZ -NIETO, AND S. A. JANSA. 2013. A New Species of Marmosops (Marsupialia: Didelphidae) from the Pakaraima Highlands of Guyana, with Remarks on the Origin of the Endemics Pantepui Mammal Fauna. American Museum Novitates 3778:1-27.
WICKHAM, H. 2016. ggplot2: Elegant Graphics for Data Anlyses. Springer-Verlag, New York, EE.UU.
WILSON, D. E. 2008. [2007]. Genus Myotis. Pp. 468-481 in Mammals of South America, Volume I Marsupials, Xenarthrans, Shrews and Bats (Gardner, A.L, ed). The University of Chicago Press, Chicago, EE.UU.
ZAR, J. H. 1998. Biostatistical analysis (4th ed). Upper Saddle River, NJ: Prentice Hall.
Published
Issue
Section
License
THERYA is based on its open access policy allowing free download of the complete contents of the magazine in digital format. It also authorizes the author to place the article in the format published by the magazine on your personal website, or in an open access repository, distribute copies of the article published in electronic or printed format that the author deems appropriate, and reuse part or whole article in own articles or future books, giving the corresponding credits.
