Revisiting species delimitation within Reithrodontomys sumichrasti (Rodentia: Cricetidae) using molecular and ecological evidence
Keywords:
Cryptic species, harvest mice, integrative taxonomy, Mesoamerican highlands, phylogeographic patternAbstract
Reithrodontomys sumichrasti is distributed from central México to Panama. Previous studies using DNA sequences suggest the existence of distinct clades that may deserve species-level recognition. Here, we use multiple methods of species delimitation to evaluate if this taxon is a complex of cryptic species. DNA sequences from the genes Cyt-b, Fgb-I7, and Acp5 were obtained from GenBank to perform molecular analyses. Species boundaries were tested using the bGMYC, STACEY, and BPP species delimitation methods. Divergence times were estimated as well as the Cyt-b genetic distances. We developed Ecological Niche Models and tested hypotheses of niche conservatism. Finally, we estimated the spatiotemporal history of lineage dispersal. The bGMYC proposed two species while STACEY and BPP proposed 4 species (genetic distances ranged from 5.43 % to 7.52 %). The ancestral position of clade I was recovered, with a Pleistocene diversification time within R. sumichrasti at ~2.15 Ma. For clade pairwise niche comparisons, the niche identity hypothesis was rejected. The ancestral distribution of R. sumichrasti was centered in Central America and spread to the west crossing the Isthmus of Tehuantepec and extending to the mountain regions of Central México. Our taxonomic considerations included the recognition of four clades as distinct species within R. sumichrasti.References
ALLEN, J. A. 1895. On the species of the genus Reithrodontomys. Bulletin of the American Museum of Natural History 7:7-143.
ALMENDRA, A. L., AND D. S. ROGERS. 2012. Biogeography of Central American mammals. Pp. 203-229, in Bones, clones, and biomes: the history and geography of recent neotropical mammals (Patterson, B. D., and L. P. Costa, eds.). University of Chicago Press. Illinois, U.S.A.
ALMENDRA, A. L., ET AL. 2018. Evolutionary relationships and climatic niche evolution in the genus Handleyomys (Sigmodontinae: Oryzomyini). Molecular Phylogenetics and Evolution 128:12-25.
ÁLVAREZ-CASTAÑEDA, S. T., ET AL. 2019. Two new species of Peromyscus from Chiapas, Mexico, and Guatemala. Pp. 543-558, in From field to laboratory: a memorial volume in honor of Robert J. Baker (Bradley, R. D., H. H. Genoways, D. J. Schmidly, and L. C. Bradley, eds.). Special Publications, Museum of Texas Tech University. Lubbock, U.S.A.
ARBOGAST, B. S., ET AL. 2002. Estimating divergence times from molecular data on phylogenetic and population genetic timescales. Annual Review of Ecology and Systematics 33:707-740.
ARELLANO, E., F. GONZÁLEZ-COZÁTL, AND D. S. ROGERS. 2005. Molecular systematics of Middle American harvest mice Reithrodontomys (Muridae), estimated from mitochondrial cytochrome b gene sequences. Molecular Phylogenetics and Evolution 37:529-540.
AVISE, J. C. 2000. Phylogeography: the history and formation of species. Harvard University Press. Massachusetts, U.S.A.
BAKER, A. J. 2008. Islands in the sky: the impact of Pleistocene climate cycles on biodiversity. Journal of Biology 7:1-4.
BAKER, R. J., AND R. D. BRADLEY. 2006. Speciation in mammals and the Genetic Species Concept. Journal of Mammalogy 87:643-662.
BANGS, O. 1902. Chiriqui Mammalia. Bulletin of the Museum of Comparative Zoology at Harvard College 39:17-51.
BIELEJEC, F., ET AL. 2011. SPREAD: spatial phylogenetic reconstruction of evolutionary dynamics. Bioinformatics 27:2910-2912.
BOUCKAERT, R., ET AL. 2014. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology 10:p.e1003537.
BRADLEY, R. D. 2017. Genus Reithrodontomys. Pp. 367-383, in Handbook of the Mammals of the World: Rodents II (Wilson, D. E., T. E. Lacher, and R. A. Mittermeier, eds.). Lynx Edicions. Barcelona, Spain.
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., ET AL. 2022. Two new species of Peromyscus (Cricetidae: Neotominae) from the Transverse volcanic belt of Mexico. Journal of Mammalogy 103:255-274.
CARSTENS, B. C., ET AL. 2013. How to fail at species delimitation. Molecular Ecology 22:4369-4383.
CEBALLOS, G., J. ARROYO-CABRALES, AND E. PONCE. 2010. Effects of Pleistocene environmental changes on the distribution and community structure of the mammalian fauna of Mexico. Quaternary Research 73:464-473.
CHIOU, K. L., ET AL. 2011. Pleistocene diversification of living squirrel monkeys (Saimiri spp.) inferred from complete mitochondrial genome sequences. Molecular Phylogenetics and Evolution 59:736-745.
CHURCH, S. A., ET AL. 2003. Evidence for multiple Pleistocene refugia in the postglacial expansion of the eastern tiger salamander, Ambystoma tigrinum tigrinum. Evolution 57:372-383.
CZAPLEWSKI, N. J. 1987. Sigmodont rodents (Mammalia; Muroidea; Sigmodontinae) from the Pliocene (early Blancan) Verde Formation, Arizona. Journal of Vertebrate Paleontology 7:183-99.
DALQUEST, W. W. 1978. Early Blancan mammals of the Beck Ranch local fauna of Texas. Journal of Mammalogy 59:269-98.
DALY, M., ET AL. 2012. Systematics Agenda 2020: the mission evolves. Systematic Biology 61:549-552.
DAYRAT, B. 2005. Towards integrative taxonomy. Biological Journal of Linnean Society 85:407-415.
DE QUEIROZ, K. 2007. Species concepts and species delimitation. Systematic Biology 56:879-886.
DELLICOUR, S., ET AL. 2021. Relax, keep walking—a practical guide to continuous phylogeographic inference with BEAST. Molecular Biology and Evolution 38:3486-3493.
DOODY, J. S., S. FREEDBERG, AND J. S. KEOGH. 2009. Communal egg-laying in reptiles and amphibians: evolutionary patterns and hypotheses. The Quarterly Review of Biology 84:229-252.
ESCALANTE, T., C. SZUMIK, AND J. J. MORRONE. 2009. Areas of endemism of Mexican mammals: reanalysis applying the optimality criterion. Biological Journal of the Linnean Society 98:468-478.
FRIENDLY, M., AND J. FOX. 2015. candisc: Visualizing generalized canonical discriminant and canonical correlation analysis. R package version 0.6-5. Available from: https://cran.r-project.org/web/packages/candisc/index.html
GILBERT, J. D., AND A. MANICA. 2015. The evolution of parental care in insects: a test of current hypotheses. Evolution 69:1255-1270.
HALL, E. R. 1981. The Mammals of North America 2nd ed. John Wiley and Sons, Inc., New York, U.S.A.
HARDY, D. K., ET AL. 2013. Molecular phylogenetics and phylogeography structure of Sumichrast´s harvest mouse (Reithrodontomys sumichrasti: Cricetidae) based on mitochondrial and nuclear DNA sequences. Molecular Phylogenetics and Evolution 68:282-292.
HEATH, T. A., J. P. HUELSENBECK, AND T. STADLER. 2014. The fossilized birth-death process for coherent calibration of divergence-time estimates. Proceedings of the National Academy of Sciences 111:2957-2966.
HELED, J., AND A. J. DRUMMOND. 2010. Bayesian inference of species trees from multilocus data. Molecular Biology and Evolution 27:570-580.
HIJMANS, R. J., ET AL. 2005. Very high-resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25:1965-1978.
HIJMANS, R. J., ET AL. 2017. Package ‘dismo’. Circles 9:1-68.
HOOPER, E. T. 1952. A systematic review of harvest mice (genus Reithrodontomys) of Latin America. Miscellaneous Publications Museum of Zoology, University of Michigan 77:1-255.
HOWES, B. J., B. LINDSAY, AND S. C. LOUGHEED. 2006. Range-wide phylogeography of a temperate lizard, the five-lined skink (Eumeces fasciatus). Molecular Phylogenetics and Evolution 40:183-194.
HUANG, J. P. 2020. Is population subdivision different from speciation? From phylogeography to species delimitation. Ecology and Evolution 10:6890-6896.
INTERNATIONAL COMMISSION ON ZOOLOGICAL NOMENCLATURE. 1999. International code of zoological nomenclature. 4th ed. International Trust for Zoological Nomenclature, London, U.K.
JOHNSON, N. K., AND C. CICERO. 2004. New mitochondrial DNA data affirm the importance of Pleistocene speciation in North American birds. Evolution 58:1122-1130.
JONES, G. 2017. Algorithmic improvements to species delimitation and phylogeny estimation under the multispecies coalescent. Journal of Mathematical Biology 74:447-467.
KATOH, K., ET AL. 2005. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research 33:511-518.
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.
KNOWLES, L. L., AND B. C. CARSTENS. 2007. Delimiting species without monophyletic gene trees. Systematic Biology 56:887-895.
KUMAR, S., ET AL. 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35:1547-1549.
LANFEAR, R., ET AL. 2014. Selecting optimal partitioning schemes for phylogenomic datasets. BMC Evolutionary Biology 14:1-14.
LEMEY, P., ET AL. 2010. Phylogeography takes a relaxed random walk in continuous space and time. Molecular Biology and Evolution 27:1877-1885.
LEÓN-PANIAGUA, L., ET AL. 2007. Diversification of the arboreal mice of the genus Habromys (Rodentia: Cricetidae: Neotominae) in the Mesoamerican highlands. Molecular Phylogenetics and Evolution 42:653-664.
LEÓNâ€TAPIA, M. Á., ET AL. 2021. Role of Pleistocene climatic oscillations on genetic differentiation and evolutionary history of the Transvolcanic deer mouse Peromyscus hylocetes (Rodentia: Cricetidae) throughout the Mexican central highlands. Journal of Zoological Systematics and Evolutionary Research 59:2481-2499.
LINDSAY, E. H., AND N. J. CZAPLEWSKI. 2011. New rodents (Mammalia, Rodentia, Cricetidae) from the Verde Fauna of Arizona and the Maxum Fauna of California, USA, early Blancan Land Mammal Age. Palaeontología Electrónica 14:1-16.
LUO, A., ET AL. 2018. Comparison of methods for molecular species delimitation across a range of speciation scenarios. Systematic Biology 67:830-846.
MAESTRI, R., ET AL. 2017. The ecology of continental evolutionary radiation: Is the radiation of sigmodontine rodents adaptive? Evolution 71:610-632.
MARTIN, P. S. 1961. Southwestern animal communities in the late Pleistocene. Biology of the arid and semiarid lands of the Southwest. New Mexico Highlands University Bulletin 212:56-66.
MARTIN, R. A., ET AL. 2002. Blancan Lagomorphs and rodents of the Deer Park assemblages, Meade County, Kansas. Journal of Paleontology 76:1072-1090.
MARTIN, R. A., ET AL. 2003. Late Pliocene and early Pleistocene rodents from the northern Borchers Badlands (Meade County, Kansas), with comments on the Blancan-Irvingtonian boundary in the Meade Basin. Journal of Paleontology 77:985-1001.
MARTIN, R. A., AND P. PELÁEZ-CAMPOMANES. 2014. Diversity dynamics of the Late Cenozoic rodent community from south-western Kansas: the influence of historical processes on community structure. Journal of Quaternary Science 29:221-231.
MARTÍNEZ-BORREGO, D., ET AL. 2022. Molecular systematics of the Reithrodontomys tenuirostris group (Rodentia: Cricetidae) highlighting the Reithrodontomys microdon species complex. Journal of Mammalogy 103:29-44.
MARTÍNEZ-GORDILLO, D., O. ROJAS-SOTO, AND A. ESPINOSA-DE LOS MONTEROS. 2010. Ecological niche modelling as an exploratory tool for identifying species limits: an example based on Mexican muroid rodents. Journal of Evolutionary Biology 23:259-270.
MERRIAM, C. H. 1901. Descriptions of 23 new harvest mice (genus Reithrodontomys). Proceedings of the Washington Academy of Sciences 3:547-558.
MORGAN, G. S, AND R. S. WHITE JR. 2005. Miocene and Pliocene vertebrates from Arizona. Pp. 114-135, in Vertebrate Paleontology in Arizona (Heckert A. B. and S. G. Lucas, eds.). New Mexico Museum of Natural History and Science Bulletin. Albuquerque, New Mexico, U.S.A.
MORRONE, J. J. 2005. Toward a synthesis of Mexican biogeography. Revista Mexicana de Biodiversidad 76:207-252.
MUSSER, G. G., AND M. D. CARLETON. 2005. Superfamily Muroidea. Pp. 894-1531, in Mammal species of the world: a taxonomic and geographic reference. 3rd ed. (D. E. Wilson and D. M. Reeder, eds.). Johns Hopkins University Press. Baltimore, U.S.A.
MYERS, N., ET AL. 2000. Biodiversity hotspots for conservation priorities. Nature 403:853-858.
ORDÓÑEZ-GARZA, N., ET AL. 2010. Patterns of phenotypic and genetic variation in three species of endemic Mesoamerican Peromyscus (Rodentia: Cricetidae). Journal of Mammalogy 91:848-859.
PADIAL, J., ET AL. 2010. The integrative future of taxonomy. Frontiers in Zoology 7:16.
PETERSON, A. T., J. SOBERÓN, AND V. SÁNCHEZ-CORDERO. 1999. Conservatism of ecological niches in evolutionary time. Science 285:1265-1267.
PHILLIPS, S. J., AND M. DUDÍK. 2008. Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31:161-175.
R DEVELOPMENT CORE TEAM. 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. www.R-project.org/
RAMBAUT, A., ET AL. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67:901-904.
RAMÍREZ-BARAHONA, S. AND L. E. EGUIARTE. 2013. The role of glacial cycles in promoting genetic diversity in the Neotropics: the case of cloud forests during the Last Glacial Maximum. Ecology and Evolution 3:725-738.
RANNALA, B. 2015. The art and science of species delimitation. Current Zoology 61:846-853.
REID, N. M., AND B. C. CARSTENS. 2012. Phylogenetic estimation error can decrease the accuracy species delimitation: a Bayesian implementation of the General Mixed Yule Coalescent model. BMC Evolutionary Biology 12:196.
RISSLER, L. J., AND J. J. APODACA. 2007. Adding more ecology into species delimitation: ecological niche models and phylogeography help define cryptic species in the black salamander (Aneides flavipunctatus). Systematic Biology 56:924-942.
ROGERS, D. S., ET AL. 2007. Molecular phylogenetic relationships among crested-tailed mice (genus Habromys). Journal of Mammalian Evolution 14:37-55.
SITES JR., J. W., AND J. C. MARSHALL. 2003. Delimiting species: a renaissance issue in systematic biology. Trends in Ecology and Evolution 18:462-470.
SITES JR., J. W., AND J. C. MARSHALL. 2004. Operational criteria for delimiting species. Annual Review of Ecology, Evolution, and Systematics 199-227.
SCHOENER, T. W. 1968. The Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology 49:704-726.
SULLIVAN, J., E. ARELLANO, AND D. S. ROGERS. 2000. Comparative phylogeography of Mesoamerican highland rodents: concerted versus independent response to past climatic fluctuations. The American Naturalist 155:755-768.
THOMAS, O. 1907. On Neotropical mammals of the genera Callicebus, Reithrodontomys, Ctenomys, Dasypus, and Marmosa. The Annals and Magazine of Natural History, 7:161-168.
URBINA, S. I., ET AL. 2006. Karyotypes of three species of harvest mice (genus Reithrodontomys). The Southwestern Naturalist 51:564-568.
WARREN, D. L., R. E. GLOR, AND M. TURELLI. 2008. Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution: International Journal of Organic Evolution 62:2868-2883.
WARREN, D. L., R. E. GLOR, AND M. TURELLI. 2010. ENMTools: a toolbox for comparative studies of environmental niche models. Ecography 33:607-611.
YANG, Z., AND B. RANNALA. 2014. Unguided species delimitation using DNA sequence data from multiple loci. Molecular Biology and Evolution 31:3125-3135.
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.
