Rejection of the monotypic status of Peromyscus furvus (Rodentia: Cricetidae), with consequences for its species group

Alejandro Cruz-Gómez, A. Alondra Castro Campillo, Zamira A. Ávila-Valle, Livia León-Paniagua, Marcia Ramírez-Sánchez, José Ramírez-Pulido

Resumen


Previous studies using Cytochrome-b or ND3-ND4 mitochondrial gene have yielded intriguing evidence about the phylogenetic relationships among populations of Peromyscus furvus; however, those studies each based on phylogenies for a single type of genes, yielded conflicting topologies.  In addition, analyses with traditional morphometrics have revealed differences in skull size among certain populations of the species.  Therefore, in order to reassess the systematic and taxonomic status of P. furvus, we incorporated a suite of genetic and morphometric characters and employed cladistic analyses.  Herein, we present results mostly derived from our genetic analyses (results from the phylogenetic examination of skull size and shape will appear later).  Phylogenetic analyses were conducted using four mitochondrial genes (Cytb and ND3-ND4L-ND4) with the respective data analyzed separately or combined, followed by an analysis with genetic and morphometric data (size and shape characters).  Most phylogenetic constructions were made with parsimonious methods, but probabilistic methods also were used in the analyses with the genes separated by type.  Similar topologies were recovered from all analyses of the Cytb gene and from all parsimony analyses of the NADH genes; however, conflicting topologies were obtained with the probabilistic methods for the NADH genes.  Additionally, to better understand the genetic variation in each type of gene, analyses for genetic divergence were conducted within and among genetic groups and haplotype networks were constructed.  All the topologies obtained using genetic data questioned the monotypic status of P. furvus, as two additional clades were identified that seemingly correspond to unrecognized entities.  The first of these, P. latirostris, occurs in the northern region and could be considered as either a species or subspecies.  An unknown Peromyscus species nova that occurs to the south is considered as a valid species.  Further, P. furvus s. s. becomes a polytypic species by recognizing at least two subspecies (P. f. angustirostris and P. f. furvus).  Phylogenetic analyses also rejected membership of P. melanocarpus and P. ochraventer within the furvus species group.  Instead, P. melanocarpus showed a greater affinity to P. mexicanus totontepecus, whereas, P. ochraventer either joined to the clade containing P. melanocarpus and P. m. tototepecus or to Megadontomys cryophilus in a sister clade.  Finally, Osgoodomys banderanus (subgenus Haplomylomys) always remained basally positioned and segregated from all members of the subgenus Peromyscus.


Palabras clave


Cytochrome-b gene; furvus species-group; multiple-character-phylogenies; NADH genes; Peromyscus.

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Referencias


ALLEN, J. A., AND F. M. CHAPMAN. 1897. On a collection of mammals from Jalapa and Las Vigas, State of Veracruz, Mexico. Bulletin of the American Museum of Natural History 9:201–203.

ÁVILA-VALLE, Z. A., A. CASTRO-CAMPILLO, AND L. LEÓN PANIAGUA. 2005. Revisión del Estado Sistemático de Peromyscus furvus (Rodentia: Muridae), México, a Partir de los Genes Mitocondriales ND3- ND4. División de Ciencias Biológicas y de la Salud, Universidad Autónoma Metropolitana, Unidad Iztapalapa. Tesis de Maestría. Ciudad de México, México.

ÁVILA-VALLE, Z. A., A. CASTRO-CAMPILLO, L. LEÓN-PANIAGUA, I. H. SALGADO-UGARTE, A. G. NAVARRO-SIGÜENZA, E. B. HERNÁNDEZ-BAÑOS, AND J. RAMÍREZ-PULIDO. 2012. Geographic variation and molecular evidence of the Blackish Deer Mouse complex (Peromyscus furvus, Rodentia: Muridae). Mammalian Biology 77:166–177.

BAKER, R. J., AND R. D. BRADLEY. 2006. Speciation in mammals and the Genetic Species Concept. Journal of Mammalogy 87:643–662

BOOKSTEIN, F. L. 1991. Morphometric Tools for Landmark Data. Geometry and Biology. Cambridge University Press. New York, U.S.A.

BRADLEY, R. D., AND R. J. BAKER. 2001. A test of the genetic species concept: Cytochrome-b sequences and mammals. Journal of Mammalogy 82:960–973.

BRADLEY, R. D., D. S. CARROLL, M. L. HAYNIE, R. M. MARTÍNEZ, M. J. HAMILTON, AND C. W. KILPATRICK. 2004a. A New Species of Peromyscus from Western Mexico. Journal of Mammalogy 85:1184–1193.

BRADLEY, R. D., N. D. DURISH, D. S. ROGERS, J. R. MILLER, M. D. ENGSTROM, AND C. W. KILPATRICK. 2007. Toward a molecular phylogeny for Peromyscus: Evidence from mitochondrial Cytochrome-b sequences. Journal of Mammalogy 88:1146–1159.

BRADLEY, R. D., C. W. EDWARDS, D. S. CARROLL, AND C. W. KILPATRICK. 2004b. Phylogenetic relationships of Neotomine–Peromyscine rodents: Based on DNA sequences from the mitochondrial Cytochrome-b gene. Journal of Mammalogy 85:389–395.

BRADLEY, R. D., N. ORDÓÑEZ-GARZA, G. CEBALLOS, D. S. ROGERS, AND D. J. SCHMIDLY. 2016. A new species in the Peromyscus boylii species group (Cricetidae: Neotominae) from Michoacán, México. Journal of Mammalogy 98:154–165.

BRADLEY, R. D., N. ORDÓÑEZ-GARZA, C. G. SOTERO-CAIO, H. M. HUYNH, C. W. KILPATRICK, L. I. IÑIGUEZ-DÁVALOS, AND D. J. SCHMIDLY. 2014. Morphometric, karyotypic, and molecular evidence for a new species of Peromyscus (Cricetidae: Neotominae) from Nayarit, Mexico. Journal of Mammalogy 95:176–186.

BRADLEY, R. D., D. J. SCHMIDLY, B. R. AMMAN, R. N. PLATT, K. M. NEUMANN, H. M. HUYNH, R. MUÑIZ-MARTÍNEZ, C. LÓPEZ-GONZÁLEZ, AND C. ORDÓÑEZ-GARZA. 2015. Molecular and morphologic data reveal multiple Species in Peromyscus pectoralis. Journal of Mammalogy 96:446–459.

CARLETON, M. D. 1989. Systematics and evolution. Pp. 7-141, in Advances in the Study of Peromyscus (Rodentia) (Kirkland, G. L., and J. N. Layne, eds.). Texas Tech University Press. Lubbock, U.S.A.

CASTAÑEDA-RICO, S. S., L. LEÓN-PANIAGUA, E. VÁZQUEZ-DOMÍNGUEZ, AND A NAVARRO-SIGÜENZA. 2014. Evolutionary diversification and speciation in rodents of the Mexican lowlands: The Peromyscus melanophrys species group. Molecular Phylogenetics and Evolution 70:454–463.

CORDEIRO-ESTREIA P., M. BAYLAC, C. DENYS, AND J. POLOP. 2008. Combining geometric morphometrics and pattern recognition to identify interspecific patterns of skull variation: Case study in sympatric Argentinian Species of the Genus Calomys (Rodentia: Cricetidae: Sigmodontinae). Biological Journal of the Linnean Society 94:365–378.

CORDERO, G. A., AND C. W. EPPS. 2012. From desert to rainforest: phenotypic variation in functionally important traits of Bushy-tailed Woodrats (Neotomacinerea) across two climatic extremes. Journal of Mammalian Evolution 19:135–153.

CRUZ-GÓMEZ A., A. CASTRO-CAMPILLO, AND L. LEÓN-PANIAGUA. 2018. Filogenia integrada de Peromyscus furvus con caracteres morfométricos y moleculares. División de Ciencias Biológicas y de la Salud, Universidad Autónoma Metropolitana, Unidad Iztapalapa. Tesis de Maestría. Ciudad de México, México.

DALQUEST, W. W. 1950. Records of mammals from the Mexican State of San Luis Potosí. Occasional Papers of the Museum of Zoology, Louisiana State University 23:1–15.

DE LUNA, E. 1995. Philosophical bases of cladistic analyses for taxonomic research. Acta Botánica Mexicana 33:63–79.

DURISH, N. D., K. E. HALCOMB, C. W. KILPATRICK, AND R. D. BRADLEY. 2004. Molecular systematics of the Peromyscus truei Species Group. Journal of Mammalogy 85:1160–1169.

EXCOFFIER, L., G. LAVAL, AND S. SCHNEIDER. 2005. Arlequin v3.0. An integrated software package for population genetics data analysis. Evolutionary Bioinformatics (online) 1:47–50.

EXCOFFIER, L., P. E. SMOUSE, AND J. M. QUATTRO. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491.

FARRIS, J. S. 1970. Methods for computing Wagner trees. Systematic Biology 19:83–92.

FELSENSTEIN, J. 2005. PHYLIP (Phylogeny Inference Package), Version 3.6. Distributed by the Author. Department of Genome Sciences, University of Washington, Seattle, WA, USA. http://evolution.genetics.washington.edu/phylip.html

GOLOBOFF, P. A., J. S. FARRIS, AND K. C. NIXON. 2008. TNT, Free Program for Phylogenetic Analysis. Cladistics 24:774–786.

GOLOBOFF, P. A., C. I. MATTONIY, AND A. S. QUINTEROS. 2006. Continuous characters analyzed as such. Cladistics 22:589–601.

GRIECO, T. M., AND O. T RIZK. 2010. Cranial shape varies along an elevation gradient in Gambel’s White‐footed Mouse (Peromyscus maniculatus gambelii) in the Grinnell Resurvey Yosemite transect. Journal of Morphology 271:897–909.

GUINDON, S., AND O. GASCUEL. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52:696–704.

HALL, E. R. 1968. Variation in the Blackish Deer Mouse, Peromyscus furvus. Anales del Instituto de Biología, Universidad Nacional Autónoma de México 1:149–154.

HALL, E. R., AND T. ÁLVAREZ. 1961. A new species of mouse (Peromyscus) from northwestern Veracruz, México. Proceedings of the Biological Society of Washington 74:203–206.

HAMMER, Ø., D. A. T. HARPER, AND P. D. RYAN. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4:9.

HARRIS, D. J., AND D. S. ROGERS. 1999. Species limits and phylogenetic relationships among populations of Peromyscus furvus. Journal of Mammalogy 80:530–544.

HARRIS, D. J., D. S. ROGERS, AND J. SULLIVAN. 2000. Phylogeography of Peromyscus furvus (Rodentia: Muridae) based on Cytochrome-b Sequence data. Molecular Ecology 9:2129–2135.

HOLMES, M. W., G. K. BOYKINS, R. C. BOWIE, AND E. A. LACEY. 2016. Cranial morphological variation in Peromyscus maniculatus over nearly a century of environmental change in three areas of California. Journal of Morphology 277:96–106.

HOOPER, E. T. 1968. Classification. Pp. 27–74, in Biology of Peromyscus (Rodentia) (King, J. A, ed.). Special Publication no 2, American Society of Mammalogists. Lawrence, U.S.A.

HUCKABY, D. G. 1980. Species limits in the Peromyscus mexicanus group (Mammalia: Rodentia: Muroidea). Contributions in Science, Natural History Museum of Los Angeles County 326:1–24.

KIMURA, M. 1980. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16:111-120.

KIMURA M. 1981. Estimation of evolutionary distances between homologous nucleotide sequences. Proceedings of the National Academy of Sciences 78:454–458.

KUMAR, S., G. STECHER, AND K. TAMURA. 2016. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets. Molecular Biological Evolution 33:1870–4.

LEDEVIN, R., AND V. MILLIEN. 2013. Congruent morphological and genetic differentiation as a signature of range expansion in a fragmented landscape. Ecology and Evolution 3:4172–4182.

LEE, M. S. Y., AND A. B. CAMENS. 2009. Strong morphological support for the molecular evolutionary tree of placental mammals. Journal of Evolutionary Biology 22:2243–2257.

LEÓN-PANIAGUA L., A. G. NAVARRO-SIGÜENZA, B. HERNÁNDEZ-BAÑOS B, AND J. C. MORALES. 2007. Diversification of the arboreal mice of the Genus Habromys (Rodentia: Cricetidae: Neotominae) in the Mesoamerican highlands. Molecular Phylogenetics and Evolution 42:653–664.

LIBRADO, P., AND J. ROZAS. 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452.

LIGHT, J. E., M. O. OSTROFF, AND D. J. HAFNER. 2016. Phylogeographic assessment of the Northern Pygmy Mouse, Baiomys taylori. Journal of Mammalogy 97:1081–1094.

LIPSCOMB D. 1998. Basics of Cladistic Analysis. George Washington University. Dstrict of Columbia, U.S.A. Available from: http://citeseerx.ist.psu.edu/viewdoc/summary?doi=10.1.1.329.9770.

LORENZO, C., S. T. ÁLVAREZ-CASTAÑEDA, S. G. PÉREZ-CONSUEGRA, AND J. L. PATTON. 2016. Revision of the Chiapan Deer Mouse, Peromyscus zarhynchus, with the description of a new Species. Journal of Mammalogy 97:910–918.

MARTÍNEZ-CORONEL, M., A. CASTRO-CAMPILLO, AND J. RAMÍREZ-PULIDO. 1997. Variación no geográfica de Peromyscus furvus (Rodentia: Muridae). Pp. 183–203, in Homenaje al Profesor Ticul Álvarez (Arroyo Cabrales, J., and O. J. Polaco, eds.). Colección Científica, Instituto Nacional de Antropología e Historia. Ciudad de México, México.

MUSSER, G. G. 1964. Notes on geographic distribution, habitat, and taxonomy of some Mexican mammals. Occasional Papers of the Museum of Zoology, University of Michigan 636:1–22.

MUSSER, G. G., AND M. D. CARLETON. 2005. Superfamily Muroidea. Pp. 894-1531, in Mammal Species of the World: A Taxonomic and Geographic Reference (Wilson, D. E, and D. M. Reed, eds.) third edition. John Hopkins University Press. Baltimore, U.S.A.

MYERS, P., B. L. LUNDRIGAN, B. W. GILLESPIE, AND M. L. ZELDITCH. 1996. Phenotypic plasticity in skull and dental morphology in the Prairie Deer Mouse (Peromyscus maniculatus bairdii). Journal of Morphology 229:229–237.

ORDÓÑEZ-GARZA, N., J. O. MATSON, R. E. STRAUSS, R. D. BRADLEY, AND J. SALAZAR-BRAVO. 2010. Patterns of phenotypic and genetic variation in three species of endemic Mesoamerican Peromyscus (Rodentia: Cricetidae). Journal of Mammalogy 91:848–859.

PERALTA-MOCTEZUMA, J. V. 2011. Estado actual de los mamíferos silvestres de la Sierra Norte de Puebla. Escuela de Biología, Benemérita Universidad Autónoma de Puebla. Tesis de Licenciatura. Puebla de los Ángeles, México.

PÉREZ-CONSUEGRA, S. E., AND E. VÁZQUEZ‐DOMÍNGUEZ. 2015. Mitochondrial diversification of the Peromyscus mexicanus Species Group in nuclear Central America: Biogeographic and taxonomic implications. Journal of Zoological Systematics and Evolutionary Research 53:300–311.

PESOLE, G., C. GISSI, A. DE CHIRICO, AND C SACCONE. 1999. Nucleotide substitution rate of mammalian mitochondrial genomes. Journal of Molecular Evolution 48:427–43.4

PLATT, R. N., B. R. AMMAN, M. S. KEITH, C. W. THOMPSON, AND R. D. BRADLEY. 2015. What is Peromyscus? Evidence from nuclear and mitochondrial DNA sequences suggests the need for a new classification. Journal of Mammalogy 96:708–719.

POSADA, D. 2008. jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution, 25:1253–1256.

RAMÍREZ-PULIDO, J., N. GONZÁLEZ-RUIZ, A. L. GARDNER, AND J. ARROYO-CABRALES. 2014. List of recent land mammals of Mexico, 2014. Special Publications, Museum of Texas Tech University 63:1-69.

RAMÍREZ-SÁNCHEZ, M., E. DE LUNA E, AND C. CRAMER. 2016. Geometric and traditional morphometrics for the assessment of character state identity: Multivariate statistical analyses of character variation in the Genus Arrenurus (Acari, Hydrachnidia, Arrenuridae). Zoological Journal of the Linnean Society 177:720–749.

ROGERS, D. S., AND J. A. SKOY. 2011. Peromyscus furvus (Rodentia: Cricetidae). Mammalian Species 43:209–215.

ROHLF, F. J. 2015. The tps series of software. Hystrix, the Italian Journal of Mammalogy 26:9-12.

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

SCOTLAND, R. W., R. G. OLMSTEAD, AND J. R. BENNETT. 2003. Phylogeny reconstruction: the role of morphology. Systematic Biology 52:539–548.

SHEETS, H. D. 2002. Morphometric Software IMP-Integrated Morphometrics Package. Department of Geology. Buffalo, U.S.A.

SHEETS, H. D., K. KIM, AND C. E. MITCHELL. 2004. A combined landmark and outline-based approach to ontogenetic shape change in the Ordovician trilobite Triarthrusbecki. Pp. 67–82, in Morphometrics–Applications in Biology and Paleontology (Elewa, A. M. T., ed.). Springer-Verlag. Heidelberg, Germany.

SOBER, E. 2004. The contest between parsimony and likelihood. Systematic Biology, 53:644–653.

STEEL, M., AND D. PENNY. 2000. Parsimony, likelihood, and the role of models in molecular phylogenetics. Molecular Biology and Evolution 17:839–850.

TAMURA, K., AND M. NEI. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10:512–526.

TAVARE, S. 1986. Some probabilistic and statistical problems in the analysis of DNA sequences. Lectures on mathematics in the life sciences 17:57–86.

TIEMANN-BOEGE, I., C. W. KILPATRICK, D. J. SCHMIDLY, AND R. D. BRADLEY. 2000. Molecular phylogenetics of the Peromyscus boylii Species Group. Molecular Phylogenetics and Evolution 16:366–378.

WADE, N. L., M. ENGSTROM, AND A. BAKER. 1999. Molecular Systematics of Neotropical Deer Mice of the Peromyscus mexicanus Species Group. Graduate Department of Zoology, University of Toronto. Master Thesis. Toronto, Canada.

WALKER, M. L., AND I. F. GREENBAUM. 2006. Mitochondrial-DNA variation and the evolutionary affinities of the Peromyscus maniculatus complex from western North America. PhD Thesis. Texas A&M University. College Station, U.S.A.

WILEY, E. O., AND R. L. MAYDEN. 2000. The evolutionary species concept. Pp. 70- 89, in Species Concepts and Phylogenetic Theory: A Debate (Wheeler, Q. D., and R.: Meier, R., eds.). Columbia University Press. New York, USA.

ZELDITCH, M. L., D. L SWIDERSKI, H. D. SHEETS, AND W. L. FINK. 2004. Geometric Morphometrics for Biologists: A Primer. Academic Press. Elsevier. Amsterdam, Neaderlands.


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