Alpha-taxonomy in the cricetid rodent Neomicroxus, a first assessment

Authors

  • Carola Cañón Instituto de Diversidad y Evolución Austral IDEAus
  • Jenny Curay Instituto Nacional de Biodiversidad INABIO
  • Jorge Brito Instituto Nacional de Biodiversidad INABIO
  • Javier Colmenares Grupo de Estudios en Biodiversidad, Universidad Industrial de Santander
  • Ulyses Pardiñas Instituto de Diversidad y Evolución Austral IDEAus

Keywords:

Andes, Colombia, Ecuador, Microxus, Neomicroxus bogotensis, Neomicroxus latebricola.

Abstract

Neomicroxus, a recently named genus, comprises small-bodied cricetid rodents patchily distributed in high-Andean ranges from Ecuador to Venezuela. Currently, two species of Neomicroxus are recognized, N. bogotensis, endemic to the Cordillera Oriental in Colombia and Cordillera de Mérida and Páramo de Tamá in Venezuela, and N. latebricola that occurs northern Andes of Ecuador. The genus is among the most poorly understood Neotropical rodents and to date no formal assessment about its alpha taxonomy was conducted. Based on DNA evidence of the first portion of the mitochondrial cytochrome b gene (cytb) and the first exon of the interphotoreceptor retinoid binding protein (IRBP), as well as craniodental measurements, we explored the divergence degree, genetic structure and phyletic relationships of the two species currently allocated under Neomicroxus. Our analyses support the monophyly of the genus as well as its uncertain tribal affiliation. Neomicroxus was retrieved as structured in two main branches, in agreement with the traditional recognition of two species. The populations referred to N. bogotensis exhibit deep divergence values (> 6 %) pointing to the existence of undescribed species under its concept. In contrast, populations of N. latebricola show a shallow genetic structure although implying recognizable geographical breaks. A moderate degree of genetic and morphological differentiation supports a new subspecies for the western populations of N. latebricola. Our contribution is the first attempt to better understanding the alpha taxonomy of Neomicroxus, highlighting the importance of the geographic complexity as a barrier to the genetic flow in N. bogotensis and the significance of the subspecies concept to formalize the geographic variation recovered in N. latebricola

References

ALARCÓN, O., G. D’ELÍA, E. P. LESSA, AND U. F. J. PARDIÑAS. 2011. Phylogeographic structure of the fossorial long-clawed mouse Chelemys macronyx (Cricetidae: Sigmodontinae). Zoological Studies 50:682–688.

ALVARADO-SERRANO, D., AND G. D’ELÍA. 2013. A new genus for the Andean mice Akodon latebricola and A. bogotensis (Rodentia: Sigmodontinae). Journal of Mammalogy 94:995–101.

ALVARADO-SERRANO, D., AND G. D’ELÍA. 2015. Genus Neomicroxus. Pp. 96–99 in Mammals of South America. Volume 2. Rodents. (J. L. Patton, J., U. F.J. Pardiñas, and G. D’Elía , eds).The University of Chicago Press. Chicago.

ANDERSON, R. P., AND P. J. SORIANO. 1999. The occurrence and biogeographic significance of the southern spiny pocket mouse Heteromys australis in Venezuela. Zeitschrift Für Säugetierkunde 64:121–125.

ANDERSON, R. P, E. E. GUTIÉRREZ, J. OCHOA-G, F. J. GARCÍA, AND M. AGUILERA. 2012. Faunal nestedness and species–area relationship for small non-volant mammals in “sky islandsâ€

of northern Venezuela. Studies on Neotropical Fauna and Environment 47:157–170.

ANTHONY, H. E. 1924. Preliminary report on Ecuadorean mammals. American Museum Novitates 6:1–9.

BARROS, M. A. AND O. REIG. 1979. Doble polimorfismo robertsoniano en Microxus bogotensis (Rodentia: Cricetidae) del páramo de Mucubají (Mérida, Venezuela). Acta Científica Venezolana 30:96.

BRITO, J. 2013. Composición y abundancia de los pequeños mamíferos terrestres en dos tipos de hábitats (Páramo de Frailejón y bosque de Polylepis) en la Reserva Ecológica El Ángel, Carchi-Ecuador. Tesis de licenciatura, Universidad Central del Ecuador, Ecuador.

CAMARGO, C., E. COLARES, AND A. M. CASTRUCCI. 2006. Seasonal pelage color change: news based on a South American rodent. Anais da Academia Brasileira de Ciências 78:77–86.

CAÑÓN, C., G. D’ELÍA, U. F. J. PARDIÑAS, AND E. P. LESSA. 2010. Phylogeography of Loxodontomys micropus with comments on the alpha taxonomy of Loxodontomys (Cricetidae: Sigmodontinae). Journal of Mammalogy 91:1449–1458.

CÁRDENAS, C. 2017. Taxonomía y distribución del género de roedores andinos: Nephelomys (Cricetidae: Sigmodontinae) en Colombia. Tesis de: Magister en Ciencias, Universidad Nacional de Colombia, Colombia.

CARLETON, M. D., AND G. G. MUSSER. 1989. Systematic Studies of Oryzomyine rodents (Muridae, Sigmodontinae): a sinopsis of Mycroryzomys. Bulletin of the American Museum of Natural History 191:1–83

CODONCODE ALIGNER V5.1. CodonCode Corporation, Centerville, Massachusetts, USA.

CORPORACIÓN SUNA HISCA. 2003. Parque Ecológico Distrital de Montaña Entrenubes, componente biofísico: Mamíferos. Bogotá D.C. 428–460.

CURAY, J. 2019. Caracterización morfométrica y modelamiento distribucional de Neomicroxus latebricola (Rodentia: Cricetidae) en el Ecuador. Tesis de licenciatura, Universidad Central del Ecuador, Ecuador.

DA SILVA, M. N. AND J. L. PATTON. 1993. Amazonian phylogeography: mtDNA sequence variation in arboreal echimyid rodents (Caviomorpha). Molecular Phylogenetics and Evolution 2:243–255.

ENDLER, J. A. 1977. Geographic variation, speciation, and clines. Monographs in Population Biology 10:1–246.

FARRIS, J. S. 1982. Simplicity and informativeness in systematics and phylogeny. Systematic Zoology 31:413–444.

FELSENSTEIN, J. 1981. Evolutionary trees from DNA-sequences; a Maximum-Likelihood approach. Journal of Molecular Evolution 17:368–376.

FITZPATRICK, J. W. 2010. Subspecies are for Convenience. Ornithological Monographs 67:54–61.

GIARLA, T. C., R. S. VOSS, AND S. A. JANSA. 2010. Species limits and phylogenetic relationships in the didelphid marsupial genus Thylamys based on mitochondrial DNA sequences and morphology. Bulletin of The American Museum of Natural History 346:1-67.

GONÇALVES P. R., A. U. CHRISTOFF, L. F. MACHADO, C. R. BONVICINO, F. B. PETERS, AND A. R. PERCEQUILLO. 2018. Unraveling Deep Branches of the Sigmodontinae Tree (Rodentia: Cricetidae) in Eastern South America. Journal of Mammalian Evolution 27:139–160.

GUARNIZO, C.E., A. PAZ, A. MUÑOZ-ORTIZ, S. V. FLECHAS, J. MÉNDEZ-NARVÁEZ, AND A.J. CRAWFORD. 2015. DNA Barcoding Survey of Anurans across the Eastern Cordillera of Colombia and the Impact of the Andes on Cryptic Diversity. PLoS ONE 10(5): e0127312.

GUTIÉRREZ, E.E., P.J. SORIANO, R.V. ROSSI, J. MURILLO, J. OCHOA-G, AND M. AGUILERA. 2011. Occurrence of Marmosa waterhousei in the Venezuelan Andes, with comments on its biogeographic significance. Mammalia 75: 381–386.

GYLDENSTOLPE, N. 1932. A manual of Neotropical sigmodont rodents. Kunglia Svenska Vetenskapsakademiens Handlingar 11:1–164.

HAMMER, Ø., D.A.T. HARPER, AND P. D. RYAN. 2001. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 4:9pp.

HANSON, J. D., AND R. D. BRADLEY. 2008. Molecular diversity within Melanomys caliginosus (Rodentia: Oryzomyini). Occasional Papers, Museum of Texas Tech University 275:1–11.

HUELSENBECK, J. P., F. RONQUIST, R. NIELSEN, AND J. BOLLBACK. 2001. Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294:2310–2314.

IRWIN, D. M., T. D. KOCHER, AND A. C. WILSON. 1991. Evolution of the cytochrome b gene of mammals. Journal of Molecular Evolution 32:128–144.

JANSA, S. A., AND R. S. VOSS. 2000. Phylogenetic Studies on Didelphid Marsupials I. Introduction and Preliminary Results from Nuclear IRBP Gene Sequences. Journal of Mammalian Evolution 7:43–77.

JOHNSON, R.A., AND D.W. WICHERN. 1999. Applied multivariate statistical analysis. Upper Saddle River, New Jersey. 67

KUMAR, S., G. STECHER, AND K. TAMURA. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33:1870–187.

LARKIN, M. A., G. BLACKSHIELDS, N. P. BROWN, R. CHENNA, P. A. MCGETTIGAN, H. MCWILLIAM, F. VALENTIN, I. M. WALLACE, A. WILM, R. LOPEZ, J. D. HOMPSON, T. J. GIBSON, D. G. HIGGINS. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948.

LINARES, O.J. 1998. Mamíferos de Venezuela. Caracas: Sociedad Conservationista Audubon de Venezuela, 691 pp.

LÓPEZ- ARÉVALO, H., O. MONTENEGRO- DÍAZ, AND A. CADENA. 1993. Ecología de los pequeños mamíferos de la Reserva Biológica Carpanta, en la Cordillera Oriental colombiana. Studies on Neotropical Fauna and Environment 28:193–210.

MORENO, P., AND L. ALBUJA. 2005. Nuevos registros de Akodon orophilus (Rodentia: Muridae) en el Ecuador. Revista Politécnica 26:28-44

MUÑOZ, G., J. CURAY, R. VITERI, M.M. GAVILÁNEZ, J. BRITO AND C. MIGUEL PINTO. 2018. El regreso de la citogenética de roedores al Ecuador: caracterización cariotípica de los ratones andinos Neomicroxus latebricola y Reithrodontomys soederstroemi. Pp 116-117 in Libro de resúmenes, II Congreso Nacional de manejo de vida silvestre y IV Congreso Ecuatoriano de Mastozoología, Loja, Ecuador.

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.

OJALA-BARBOUR, R., J. BRITO, AND W. TESKA. R. 2019. A comparison of small mammal communities in two High-Andean Polylepis woodlands in Ecuador. ACI Avances en Ciencias e Ingenierías 11:208–221.

PALMA, R. E., E. RODRÍGUEZ-SERRANO, E. RIVERA-MILLA, C. E HERNÁNDEZ, J. SALAZAR-BRAVO, CARMA, M. I., T. L. YATES. 2010. Phylogenetic relationships of the pygmy rice rats of the genus Oligoryzomys Bangs, 1900 (Rodentia: Sigmodontinae). Zoological Journal of the Linnean Society of London 160:551–566.

PALMA, E., AND E. RODRÍGUEZ-SERRANO. 2017. Systematics of Oligoryzomys (Rodentia, Cricetidae, Sigmodontinae) from southern Chilean Patagonia, with the description of a new species. Journal of Zoological Systematics and Evolutionary Research 1–21.

PARDIÑAS, U. F. J., AND J. BRITO. 2017. Genus Neomicroxus. Pp 409 in Handbook of the Mammals of the World-Volume 7: Rodents II. (D. E. Wilson, T. E. Lacher, Jr., and R. A. Mittermeier eds). Lynx Editions.

PATTON, J. L., P. MYERS, AND M. F. SMITH. 1990. Vicariant versus gradient model of diversification: the small mammal fauna of eastern Andean slopes of Peru. Pp 355–371 in Vertebrates in the Tropics (Peters, G., and R. Hutterer eds). Bonn: Alexander Koenig Zoological Research Institute.

PATTON, J.L., AND C.J. CONROY. 2017. The conundrum of subspecies: morphological diversity among desert populations of the California vole (Microtus californicus, Cricetidae). Journal of Mammalogy 98:1010–1026.

POSADA, D. 2008. jModelTest: Phylogenetic Model Averaging. Molecular Biology and Evolution. 25(7):1253–1256.

RAMBAUT, A., A. J. DRUMMOND, D. XIE, G. BAELE, AND M. A. SUCHARD. 2018. Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67:901–904.

RAMÍREZ-CHAVES, H. E., AND E. A. NOGUERA-URBANO. 2010. Lista preliminar de los mamíferos (Mammalia: Theria) del departamento de Nariño, Colombia. Biota Colombiana 11:117–140.

REIG, O. 1986. Diversity patterns and differentiation of high Andean rodents. Pp 404–40 in High Altitude Tropical Biogeography, (Vuilleumier, F., and M. Monasterio eds). New York: Oxford University Press.

REIG, O. 1987. An assessment of the systematics and evolution of the Akodontini, with the description of new fossil species of Akodon (Cricetidae: Sigmodontinae). Fieldiana: Zoolology 39:347–399.

RIOS, E., AND S. T. ÁLVAREZ-CASTAÑEDA. 2012. Pelage color variation in pocket gophers (Rodentia: Geomyidae) in relation to sex, age and differences in habitat. Mammalian Biology 77:160–165.

RONQUIST, F., M. TESLENKO, P. VAN DER MARK, D.L. AYRES, A. DARLING, S. HÖHNA, B. LARGET, L. LIU, M. A. SUCHARD, AND J. P. HUELSENBECK. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology. 61:539–542.

SÁENZ-JIMÉNEZ, F.A. 2010. Aproximación a la fauna asociada a los bosques de roble del corredor Guantiva – La Rusia – Iguaque (Boyacá–Santander, Colombia). Revista Colombia Forestal 13:299–334.

SANDOVAL SALINAS, M. L., R. M. BÁRQUEZ, E. M. COLOMBO, AND J. D. SANDOVAL. 2017. Intra-specific pelage color variation in a South American small rodent species. Brazilian Journal of Biology 77:1–11.

SALAZAR-BRAVO J., U.F.J. PARDIÑAS, H. ZEBALLOS, AND P. TETA. 2016. Description of a new tribe of Sigmodontinae rodents (Cricetidae: Sigmodontinae) with an updated summary of valid tribes and their generic contents. Occasional Paper Museum Texas Tech University 338:1–24.

SMITH, M. F. AND J. L. PATTON. 1993. The diversification of South American murid rodents: evidence from mitochondrial DNA sequence data for the akodontine tribe. Biological Journal of the Linnean Society 50:149–177.

SORIANO, P. J., A. DÍAZ DE PASCUAL, J. OCHOA-G., AND M. AGUILERA. 1999. Biogeographic analysis of the mammal communities in the Venezuelan Andes. Interciencia 24:17–25.

SORIANO, P.J., A. RUIZ, AND Z. ZAMBRANO. 2005. New noteworthy records of bats for the Andean region of Venezuela and Colombia. Mammalia 69:251–255.

STANHOPE, M., J., J. CZELUSNIAK, J-S. SI, J. NICKERSON, AND M. GOODMAN. 1992. A molecular perspective on mammalian evolution from the gene encoding Interphotoreceptor Retinoid Binding Protein, with convincing evidence for bat monophyly. Molecular Phylogenetics and Evolution 1:148–160.

STEPPAN, S. J., R. M. ASKINS, AND J. ANDERSON. 2004. Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Systematic Biology 53:533–553.

SWOFFORD, D. L. 2000. PAUP*: Phylogenetics Analysis Using Parsimony (*and Other Methods). Ver. 4.0. [Computer software and manual]. Sunderland, MA: Sinauer Associates, Inc. Publishers.

THOMAS, O. 1895. On small mammals from Nicaragua and Bogota. Annals and Magazine of Natural History 6:55–60.

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:W232–W235.

VENTURA, J., M.J. LÓPEZ-FUSTER, M. SALAZAR, AND R. PÉREZ-HERNANDEZ. 2000. Morphometric analysis of some Venezuelan akodontine rodents. Netherlands Journal of Zoology 50: 487–501.

VIANCHÁ SÁNCHEZ, A., J. CEPEDA-GÓMEZ, E. MUÑOZ LÓPEZ, A. HERNÁNDEZ OCHIA, AND L. ROSERO LASPRILLA. 2012. Mamíferos pequeños no voladores del Parque Natural Municipal Ranchería, Paipa, Boyacá, Colombia. Biodiversidad Neotropical 2:37–44.

VOSS, R. S. 2003. A new species of Thomasomys (Rodentia: Muridae) from eastern Ecuador, with remarks on mammalian diversity and biogeography in the Cordillera Oriental. American Museum Novitates 3421:1–47.

VOSS, R., AND A.V. LINZEY. 1981. Comparative Gross Morphology of Male Accessory Glands among Neotropical Muridae (Mammalia: Rodentia) with Comments on Systematic Implications. Miscellaneous publications Museum of Zoology, University of Michigan 159:1–41.

WILSON, E. O, AND W. L. BROWN. 1953. The subspecies concept and its taxonomic application. Systematic Biology 2:97–111.

Downloads

Published

2020-08-22

Issue

Section

Special Contribution