Paraphyletic relationships revealed by mitochondrial DNA in the Peromyscus mexicanus species group (Rodentia: Cricetidae)

Autores/as

  • Giovani Hernández-Canchola Louisiana State University https://orcid.org/0000-0002-5874-6919
  • Livia León-Paniagua Universidad Nacional Autónoma de México
  • Jacob A. Esselstyn Louisiana State University

DOI:

https://doi.org/10.22201/ib.20078706e.2022.93.3811

Palabras clave:

Teapensis, Tehuantepecus, Totontepecus, Filogenia molecular, Cytochromo b

Resumen

Although deer mice (Peromyscus spp.) are among the most studied small mammals, their species diversity and phylogenetic relationships remain unclear. The lack of taxonomic clarity is mainly due to a conservative morphology and because some taxa are rare, have restricted distributions, or are poorly sampled. One taxon, P. mexicanus, includes southern Mexican subspecies that have not had their systematic placement tested with genetic data. We analyzed the phylogenetic relationships and genetic structure of P. mexicanus populations using sequences of the mitochondrial gene cytochrome b. We inferred that P. mexicanus is paraphyletic, with P. m. teapensis, P. m. tehuantepecus, andP. m. totontepecus more closely related to P. gymnotis than to P. m. mexicanus. This highly divergent clade ranges from northeastern Oaxaca to northern Chiapas, including southern Veracruz, and southern Tabasco. In light of this group’s mitochondrial distinctiveness, cohesive geographic range, and previously reported molecular, biochemical, and morphological differences, we recommend it be treated as P. totontepecus. Our findings demonstrate the need for an improved understanding of the diversity and evolutionary history of these common and abundant members of North American small mammal communities.

Biografía del autor/a

Giovani Hernández-Canchola, Louisiana State University

Becario posdoctoral en el Museum of Natural Science, Louisiana State University

Citas

Álvarez-Castañeda, S. T., Álvarez, T., & González-Ruiz, N. (2015). Guía para la identificación de los mamíferos de México en campo y laboratorio. Guadalajara: Centro de Investigaciones del Noroeste, S. C./ Asociación Mexicana de Mastozoología, A. C.

Álvarez-Castañeda, S. T., Lorenzo, C., Segura-Trujillo, C. A., & Pérez-Consuegra, S. G. (2019). Two new species of Peromyscus from Chiapas, Mexico, and Guatemala. In R. D. Bradley, H. H. Genoways, D. J. Schmidly, & L. C. Bradley (Eds.), From field to laboratory: a memorial volume in honor to Robert J. Baker (pp. 543–558). Special Publications 71. Lubbock, TX: Museum of Texas Tech University.

Arellano, E., González-Cozátl, F. X., & Rogers, D. S. (2005). Molecular systematics of Middle American harvest mice Reithrodontomys (Muridae), estimated from mitochondrial cytochrome b gene sequences. Molecular Phylogenetics and Evolution, 37, 529–540. https://doi.org/10.1016/j.ympev.2005.07.021

Ávila-Valle, Z. A., Castro-Campillo, A., León-Paniagua, L., Salgado-Ugalde, I. H., Navarro-Sigüenza, A. G., Hernández-Baños, B. E. et al. (2012). Geographic variation and molecular evidence of the blackish deer mouse complex (Peromyscus furvus, Rodentia: Muridae). Mammalian Biology, 77, 166–177. https://doi.org/10.1016/j.mambio.2011.09.008

Bradley, R. D., Durish, N. D., Rogers, D. S., Miller, J. R., Engstrom, M. D., & Kilpatrick, C. W. (2007). Toward a molecular phylogeny for Peromyscus: evidence from mitochondrial cytochrome- b sequences. Journal of Mammalogy, 88, 1146–1159. https://doi.org/10.1644/06-mamm-a-342r.1

Bradley, R. D., Edwards, C. W., Carroll, D. S., & Kilpatrick, C. W. (2004). Phylogentic relationships of neotomine-peromyscine rodents: based on DNA sequencues from the mitochondrial cytochrome-b gene. Journal of Mammalogy, 85, 389–395. https://doi.org/10.1644/ber-026

Bradley, R. D., Francis, J. Q., Platt, R. N., Soniat, T. J., Alvarez, D., & Lindsey, L. L. (2019). Mitochondrial DNA sequence data indicate evidence for multiple species within Peromyscus maniculatus (Issue 70). Lubbock, TX: Museum of Texas Tech University. https://doi.org/10.1098/rsnr.1961.0025

Bradley, R. D., Ordóñez-Garza, N., Ceballos, G., Rogers, D. S., & Schmidly, D. J. (2017). A new species in the Peromyscus boylii species group (Cricetidae: Neotominae) from Michoacán, México. Journal of Mammalogy, 98, 154–165. https://doi.org/10.1093/jmammal/gyw160

Carleton, M. D. (1980). Phylogenetic relationships in neotomine-peromyscine rodents (Muroidea) and a reappraisal of the dichotomy within New World Cricetinae. Miscellaneous Publications Museum of Zoology, University of Michigan, 157, 1–146.

Carleton, M. D. (1989). Systematics and evolution. In G. L. J. Kirkland, & J. N. Layne (Eds.), Advances in the study of Peromyscus (Rodentia) (pp. 7–141). Lubbock, TX: Texas Tech University Press.

Castañeda-Rico, S., León-Paniagua, L., Vázquez-Domínguez, E., & Navarro-Sigüenza, A. G. (2014). Evolutionary diversification and speciation in rodents of the Mexican lowlands: the Peromyscus melanophrys species group. Molecular Phylogenetics and Evolution, 70, 454–463. https://doi.org/10.1016/j.ympev.2013.10.004

Cortés-Rodríguez, N., Jacobsen, F., Hernández-Baños, B. E., Navarro-Sigüenza, A. G., Peters, J. L., & Omland, K. E. (2013). Coalescent analyses show isolation without migration in two closely related tropical orioles: the case of Icterus graduacauda and Icterus chrysater. Ecology and Evolution, 3, 4377–4387. https://doi.org/10.1002/ece3.768

Durish, N. D., Halcomb, K. E., Kilpatrick, C. W., & Bradley, R. D. (2004). Molecular systematics of the Peromyscus truei species group. Journal of Mammalogy, 85, 1160–1169. https://doi.org/10.1644/ber-115.1

Excoffier, L., & Lischer, H. E. L. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x

Goodwin, G. G. (1956). Seven new mammals from México. American Museum Novitates, 1791, 1–10.

Goodwin, G. G. (1964). A new species and a new subspecies of Peromyscus from Oaxaca, Mexico. American Museum Novitates, 2183, 1–8.

Greenbaum, I. F., Honeycutt, R. L., & Chirhart, S. E. (2019). Taxonomy and phylogenetics of the Peromyscus maniculatus species group. In R. D. Bradley, H. H. Genoways, D. J. Schmidly, & L. C. Bradley (Eds.), From field to laboratory: a memorial volume in honor to Robert J. Baker (pp. 559–575). Special Publications 71. Lubbock, TX: Museum of Texas Tech University.

Guevara, L., & Cervantes, F. A. (2014). Molecular systematics of small-eared shrews (Soricomorpha, Mammalia) within Cryptotis mexicanus species group from Mesoamérica. Acta Theriologica, 59, 233–242. https://doi.org/10.1007/s13364-013-0165-6

Guevara, L., Sánchez-Cordero, V., León-Paniagua, L., & Woodman, N. (2014). A new species of small-eared shrew (Mammalia, Eulipotyphla, Cryptotis) from the Lacandona rain forest, Mexico. Journal of Mammalogy, 95, 739–753. https://doi.org/10.1644/14-mamm-a-018

Hernández-Canchola, G., & León-Paniagua, L. (2021). About the specific status of Baiomys musculus and B. brunneus. Therya, 12, 291–301. https://doi.org/10.12933/therya-21-1150

Hernández-Canchola, G., León-Paniagua, L., & Esselstyn, J. A. (2021). Mitochondrial DNA indicates paraphyletic relationships of disjunct populations in the Neotoma mexicana species group. Therya, 12, 411–421. https://doi.org/10.12933/therya-21-1082

Hsu, T. C., & Arrighi, F. E. (1966). Chromosomal evolution in the genus Peromyscus (Cricetidae, Rodentia). Cytogenetics, 5, 355–359.

Irwin, D. M., Kocher, T. D., & Wilson, A. C. (1991). Evolution of the cytochrome b gene of mammals. Journal of Molecular Evolution, 32, 128–144.

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., & Tamura, 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

Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T., & Calcott, B. (2016). PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34, 772–773.

León-Paniagua, L., Navarro-Sigüenza, A. G., Hernández-Baños, B. E., & Morales, J. C. (2007). Diversification of the arboreal mice of the genus Habromys (Rodentia: Cricetidae: Neotominae) in the Mesoamerican highlands. Molecular Phylogenetics and Evolution, 42, 653–664. https://doi.org/10.1016/j.ympev.2006.08.019

León-Tapia, M. Á. (2013). Ubicación filogenética con caracteres moleculares de la rata de monte (Nelsonia goldmani), endémica del Eje Neovolcánica Transversal (Master Thesis). Universidad Nacional Autónoma de México, Mexico City, Mexico.

León-Tapia, M. Á., Fernández, J. A., Rico, Y., Cervantes, F. A., & Espinosa-de los Monteros, A. (2020). A new mouse of the Peromyscus maniculatus species complex (Cricetidae) from the highlands of central Mexico. Journal of Mammalogy, 101, 1117–1132. https://doi.org/10.1093/jmammal/gyaa027

Librado, P., & 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

López-González, C., García-Mendoza, D. F., López-Vidal, J. C., & Elizalde-Arellano, C. (2019). Multiple lines of evidence reveal a composite of species in the plateau mouse, Peromyscus melanophrys (Rodentia, Cricetidae). Journal of Mammalogy, 100, 1583–1598. https://doi.org/10.1093/jmammal/gyz106

Lorenzo, C., Álvarez-Castañeda, S. T., Pérez-Consuegra, S. G., & Patton, J. L. (2016). Revision of the Chiapan deer mouse, Peromyscus zarhynchus, with the description of a new species. Journal of Mammalogy, 97, 910–918. https://doi.org/10.1093/jmammal/gyw018

Merriam, C. H. (1898). Descriptions of twenty new species and a new subgenus of Peromyscus from Mexico and Guatemala. Proceedings of the Biological Society of Washington, 12, 115–125.

Miller, J. R., & Engstrom, M. D. (2008). The relationships of major lineages within peromyscine rodents: a molecular phylogenetic hypothesis and systematic reappraisal. Journal of Mammalogy, 89, 1279–1295. https://doi.org/10.1644/07-mamm-a-195.1

Nguyen, L. T., Schmidt, H. A., von Haeseler, A., & Minh, B. Q. (2015). IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 32, 268–274. https://doi.org/10.1093/molbev/msu300

Ordóñez-Garza, N., Matson, J. O., Strauss, R. E., Bradley, R. D., & Salazar-Bravo, J. (2010). Patterns of phenotypic and genetic variation in three species of endemic Mesoamerican Peromyscus (Rodentia: Cricetidae). Journal of Mammalogy, 91, 848–859. https://doi.org/10.1644/09-mamm-a-167.1

Osgood, W. H. (1904). Thirty new mice of the genus Peromyscus from Mexico and Guatemala. Proceedings of the Biological Society of Washington, 17, 55–77.

Osgood, W. H. (1909). Revision of the mice of the American genus Peromyscus. North American Fauna, 28, 1–285.

Pardiñas, U., Myers, P., León-Paniagua, L., Ordóñez-Garza, N., Cook, J., Kryštufek, B. et al. (2017). Family Cricetidae (true hamsters, voles, lemmings and new world rats and mice). In D. E. Wilson, R. A. Mittermeier, & T. E. Lacher (Eds.), Handbook of the mammals of the World. Volume 7 Rodents II (pp. 204–279). Barcelona: Lynx Edicions.

Patterson, J., Chamberlain, B., & Thayer, D. (2004). Finch TV Version 1.4.0. Published by authors.

Pérez-Consuegra, S. G., & Vázquez-Domínguez, E. (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. https://doi.org/10.1111/jzs.12099

Pérez-Consuegra, S. G., & Vázquez-Domínguez, E. (2017). Intricate evolutionary histories in montane species: a phylogenetic window into craniodental discrimination in the Peromyscus mexicanus species group (Mammalia: Rodentia: Cricetidae). Journal of Zoological Systematics and Evolutionary Research, 55, 57–72. https://doi.org/10.1111/jzs.12155

Platt, R. N., Amman, B. R., Keith, M. S., Thompson, C. W., & Bradley, R. D. (2015). What is Peromyscus? Evidence from nuclear and mitochondrial DNA sequences suggests the need for a new classification. Journal of Mammalogy, 96, 708–719. https://doi.org/10.1093/jmammal/gyv067

Rambaut, A., Drummond, A. J., Xie, D., Baele, G., & Suchard, M. A. (2018). Posterior summarization in bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67, 901–904. https://doi.org/10.1093/sysbio/syy032

Ramírez-Pulido, J., Arroyo-Cabrales, J., & Castro-Campillo, A. (2005). Estado actual y relación nomenclatural de los mamíferos terrestres de México. Acta Zoológica Mexicana, 21, 21–82. https://doi.org/10.21829/azm.2005.2112008

Ramírez-Pulido, J., González-Ruiz, N., Gardner, A. L., & Arroyo-Cabrales, J. (2014). List of recent land mammals of Mexico, 2014. Special Publications 63. Lubbock, TX: The Museum Tech University.

Rogers, D. S., & Engstrom, M. D. (1992). Evolutionary implications of allozymic variation in tropical Peromyscus of the mexicanus species group. Journal of Mammalogy, 73, 55–69.

Rogers, D. S., Funk, C. C., Miller, J. R., & Engstrom, M. D. (2007). Molecular phylogenetic relationships among crested-tailed mice (genus Habromys). Journal of Mammalian Evolution, 14, 37–55. https://doi.org/10.1007/s10914-006-9034-2

Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Höhna, S. et al. (2012). Mrbayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542. https://doi.org/10.1093/sysbio/sys029

Schliep, K. P. (2011). phangorn: phylogenetic analysis in R. Bioinformatics, 27, 592–593. https://doi.org/10.1093/bioinformatics/btq706

Shimodaira, H., & Hasegawa, M. (1999). Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution, 16, 1114–1116. https://doi.org/10.1111/j.1467-789X.2009.00675.x

Smith, M. F., & Patton, J. L. (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. https://doi.org/10.1111/j.1095-8312.1993.tb00924.x

Stangl, F. B., & Baker, R. J. (1984). Evolutionary relationships in Peromyscus: congruence in chromosomal, genic, and classical data sets. Journal of Mammalogy, 65, 643–654.

Sullivan, J., Markert, J. A., & Kilpatrick, C. W. (1997). Phylogeography and molecular systematics of the Peromyscus aztecus species group (Rodentia: Muridae) inferred using parsimony and likelihood. Systematic Biology, 46, 426–440. https://doi.org/10.1093/sysbio/46.3.426

Sullivan, K. A. M., Platt, R. N., Bradley, R. D., & Ray, D. A. (2017). Whole mitochondrial genomes provide increased resolution and indicate paraphyly in deer mice. BMC Zoology, 2, 1–6. https://doi.org/10.1186/s40850-017-0020-3

Trujano-Álvarez, A. L., & Álvarez-Castañeda, S. T. (2010). Peromyscus mexicanus (Rodentia: Cricetidae). Mammalian Species, 42, 111–118. https://doi.org/10.1644/858.1

Vallejo, R. M., & González-Cózatl, F. X. (2012). Phylogenetic affinities and species limits within the genus Megadontomys (Rodentia: Cricetidae) based on mitochondrial sequence data. Journal of Zoological Systematics and Evolutionary Research, 50, 67–75. https://doi.org/10.1111/j.1439-0469.2011.00634.x

Wade, N. L. (1999). Molecular systematics of Neotropical deer mice of the Peromyscus mexicanus species group (Master Thesis). University of Toronto, Toronto, Canada.

Wickham, H. (2011). ggplot2. Wiley Interdisciplinary Reviews: Computational Statistics, 3, 180–185. https://doi.org/10.1002/wics.147

Woodman, N., & Timm, R. M. (1999). Geographic variation and evolutionary relationships among broad-clawed shrews of the Cryptotis goldmani-group (Mammalia: Insectivora: Soricidae). Fieldiana: Zoology (New Series), 91, 1–35. https://doi.org/10.5962/bhl.title.2669

Zaragoza-Quintana, E. P. (2005). Variación geográfica de Peromyscus mexicanus (Rodentia: Muridae) en México (Bachelor Thesis). Universidad Nacional Autónoma de México, Mexico City, Mexico.

Descargas

Publicado

2022-08-19

Número

Sección

TAXONOMÍA Y SISTEMÁTICA