An 1896 specimen helps clarify the phylogenetic placement of the Mexican endemic Hooper’s deer mouse
Keywords:
Historical DNA, genomics, mitogenomes, museum specimens, Peromyscus, Pliocene-Pleistocene, ultraconserved elements.Abstract
Hooper’s deer mouse, Peromyscus hooperi, is the sole member of the Peromyscus hooperi species group. This species is endemic to México where it is restricted to the grassland transition zone in the states of Coahuila, Zacatecas, and San Luis Potosí. Previous studies using mitochondrial and nuclear genes (Cytb, Adh1-I2, Fgb-I7 and Rbp3) did not resolve the phylogenetic relationships of this relatively poorly known species. It was hypothesized that P. hooperi is sister to P. crinitus, and these two taxa are related to P. melanotis, P. polionotus, P. maniculatus, P. keeni, P. leucopus, P. gossypinus, P. eremicus, P. californicus, and Osgoodomys banderanus. Based on morphological characters, karyotypes, and allozymes, P. hooperi does not align with either subgenera Haplomylomys or Peromyscus. However, its unique characteristics (e. g., phallus, karyotype) have been recognized, and therefore it has been retained as its own species group. To better resolve the phylogenetic placement of P. hooperi, we performed target-enrichment and high-throughput sequencing and obtained several thousand nuclear ultraconserved elements and a complete mitogenome from a specimen collected in 1896 by Nelson and Goldman in Coahuila, México. We compared these data with 21 other species of neotomines using genome-wide data. Contrary to previous studies, we found high nodal support for the placement of P. hooperi as sister to a clade that includes Podomys floridanus, Neotomodon alstoni, Habromys simulatus, H. ixtlani, Peromyscus mexicanus, P. megalops, P. melanophrys, P. perfulvus, P. aztecus, P. attwateri, P. pectoralis, and P. boylii. We dated a Pliocene divergence of P. hooperi from its sister group at approximately 3.98 mya, and after the split of P. crinitus at ca. 4.31 mya from other peromyscines. We demonstrated that genome-wide data improve the phylogenetic signal, independently of taxon sampling, for a phylogenetically problematic species such as P. hooperi. We recommend that future genomic studies expand taxon sampling, including members of the subgenus Haplomylomys, to confirm the phylogenetic relationships of P. hooperi and the genetic status of its populations.References
Abreu-Jr., E. F., et al. 2020. Museomics of tree squirrels: a dense taxon sampling of mitogenomes reveals hidden diversity, phenotypic convergence, and the need of a taxonomic overhaul. BMC Evolutionary Biology 20:77.
Andrews, S. 2010. FastQC: A Quality Control Tool For High Throughput Sequence Data. http://www.bioinformatics.babraham.ac.uk/projects/ fastqc
Álvarez-Castañeda, S. T. 2002. Peromyscus hooperi. Mammalian Species 709:1–3.
Álvarez-Castañeda, S. T. 2016. Peromyscus hooperi. in IUCN 2022. The IUCN Red List of Threatened Species. Version 2022-1. www.iucnredlist.org Accessed on 22 August 2022.
Bonilla-Moheno, M., and T. M. Aide. 2020. Beyond deforestation: Land cover transition in Mexico. Agricultural System 178:102734.
Bradley, R. D., et al. 2007. Toward a molecular Phylogeny for Peromyscus: evidence from mitochondrial cytochrome-b sequences. Journal of Mammalogy 88:1146–1159.
Bradley, R. D., et al. 2019. Mitochondrial DNA sequence data indicate evidence for multiple species within Peromyscus maniculatus. Special Publications Museum of Texas Tech University 70:1–68.
Bouckaert, R., et al. 2019. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Computational Biology 15:e1006650.
Campana, M. G. 2019. uce2speciestree. https://github.com/campanam/uce2speciestree. Accessed on 22 August 2022.
Card, D. C., et al. 2021. Museum Genomics. Annual Review of Genetics 55:633–659.
Carleton, M. D. 1980. Phylogenetic relationships in Neotomine– Peromyscine rodents (Muridae) and a reappraisal of the dichotomy within New World Cricetinae. Miscellaneous Publications of the Museum of Zoology, University of Michigan 157:1–146.
Carleton, M. D. 1989. Systematics and evolution. Pp. 7–141, in Advances in the study of Peromyscus (Rodentia) (G. L. Kirkland, Jr. and J. N. Layne, eds.). Texas Tech University Press, Lubbock, USA.
Castañeda-Rico, S., et al. 2014. Evolutionary diversification and speciation in rodents of the Mexican lowlands: the Peromyscus melanophrys species group. Molecular Phylogenetics and Evolution 70:454–463.
Castañeda-Rico, S., et al. 2020. Ancient DNA From Museum Specimens and Next Generation Sequencing Help Resolve the Controversial Evolutionary History of the Critically Endangered Puebla Deer Mouse. Frontiers in Ecology and Evolution 8:94.
Castañeda-Rico, S., et al. 2022. Museomics and the holotype of a critically endangered cricetid rodent provide key evidence of an undescribed genus. Frontiers in Ecology and Evolution 10:930356.
Cornejo-Latorre, C., et al. 2017. The evolutionary history of the subgenus Haplomylomys (Cricetidae: Peromyscus). Journal of Mammalogy 98:1627-1640.
Dalquest, W. W. 1962. The Good Creek formation, Pleistocene of Texas, and its fauna. Journal of Paleontology 36:568–582.
Darriba, D., et al. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9:772.
Dawson, W. 2005. Peromyscine biogeography, Mexican topography and Pleistocene climatology. Pp. 145–156, in Contribuciones Mastozoológicas en Homenaje a Bernardo Villa (V. Sánchez-Cordero and R. Medellín, eds.). UNAM-CONABIO, Ciudad de México, México.
Duchêne, S., et al. 2011. Mitogenome phylogenetics: The impact of using single regions and partitioning schemes on topology, substitution rate and divergence time estimation. PLoS ONE. 6:e27138.
Faircloth, B. C. 2013. Illumiprocessor: a Trimmomatic wrapper for parallel adapter and quality trimming. doi: 10.6079/J9ILL
Faircloth, B. C. 2016. PHYLUCE is a software package for the analysis of conserved genomic loci. Bioinformatics 32:786–788.
Fuller, B., et al. 1984. Albumin evolution in Peromyscus and Sigmodon. Journal of Mammalogy 65:466–473.
Galván-Miyoshi, Y., et al. 2015. Land Change Regimes and the Evolution of the Maize-Cattle Complex in Neoliberal Mexico. Land 4:754–777.
Grabherr, M. G., et al. 2011. Full-length transcriptome assembly from RNA-seq data without a reference genome. Nature Biotechnology 29:644–652.
Guevara, L. The legacy of the fieldwork of E. W. Nelson and E. A. Goldman in Mexico (1892–1906) for research on poorly known mammals. 2021. History and Philosophy of the Life Sciences 43:31.
Guindon, S., and O. Gascuel. 2003. A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology 52:696–704.
Heled, J., and A. J. Drummond. 2012. Calibrated tree priors for relaxed phylogenetics and divergence time estimation. Systematic Biology 61:138–149.
Hibbard, C.W. 1968. Paleontology. Pp. 6–26, in Biology of Peromyscus (Rodentia) (King, J. A., ed.). Special Publication 2, American Society of Mammalogist, Oklahoma, USA.
Hogan, K., et al. 1993. Systematic and taxonomic implications of karyotypic, electrophoretic and mitochondrial DNA variation in Peromyscus from the Pacific Northwest. Journal of Mammalogy 74:819–831.
Hooper, E. T. 1968. Classification. Pp. 27–74, in Biology of Peromyscus (Rodentia) (J. A. King, ed.). Special Publication 2, The American Society of Mammalogists, Oklahoma, USA.
Hooper, E. T., and G. G. Musser. 1964. Notes on classification of the rodent genus Peromyscus. Occasional Papers of the Museum of Zoology, University of Michigan 635:1–13.
Huelsenbeck, J. P., and F. Ronquist. 2001. MRBAYES: bayesian inference of phylogeny. Bioinformatics 17:754–755.
Jónsson, H., et al. 2013. mapDamage2.0: fast approximate Bayesian estimates of ancient DNA damage parameters. Bioinformatics 13:1682–1684.
Karow, P. F., et al. 1996. Middle Pleistocene (early Rancholabrean) vertebrates and associated marine and non-marine invertebrates from Oldsmar, Pinellas County, Florida. Pp. 97–133, in Palaeoecology and palaeoenvironments of Late Cenozoic mammals: Tributes to the career of C. S. (Rufus) Churcher (K. Stewart and K. Seymour, eds.). University of Toronto Press, Toronto, Canada.
Katoh, K., and D. M. Standley. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30:772–780.
Lanfear, R., et al. 2016. PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34:772–773.
Lee, M. R., and D. J. Schmidly. 1977. A new species of Peromyscus (Rodentia: Muridae) from Coahuila, Mexico. Journal of Mammalogy 58:263–268.
León-Tapia, M.A., 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.
López-Medellín, X., and R. Medellín. 2016. The influence of E. W. Nelson and E. A. Goldman on Mexican Mammalogy. Special Publications Museum of Texas Tech University 64:87–103.
McDonough, M. M., et al. 2018. Performance of commonly requested destructive museum samples for mammalian genomic studies. Journal of Mammalogy 99:789–802.
McDonough, M. M., et al. 2022. Phylogenomic systematics of the spotted skunks (Carnivora, Mephitidae, Spilogale): Additional species diversity and Pleistocene climate change as a major driver of diversification. Molecular Phylogenetic and Evolution 167:107266.
Meyer, M., and M. Kircher. 2010. Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harbor Protocols 2010:pdb.prot5448.
Miller, J. R., and M. D. Engstrom. 2008. The relationships of major lineages within peromyscine rodents: a molecular phylogenetic hypothesis and systematic reappraisal. Journal of Mammalogy 89:1279–1295.
Musser, G., and M. D. Carleton. 1993. Family Muridae. Pp. 501–755, in Mammal Species of the World: A Taxonomic and Geographic Reference (Wilson, D. E., and M. Reeder, eds.). Smithsonian Institution Press, Washington DC, USA.
Musser, G., and M. D. Carleton. 2005. Superfamily Muridae. Pp. 894–1531, in Mammal Species of the World: A Taxonomic and Geographic Reference (Wilson, D. E., and M. Reeder, eds.). Johns Hopkins University Press, Baltimore, USA.
Nakamura, T., et al. 2018. Parallelization of MAFFT for large-scale multiple sequence alignments. Bioinformatics 34:2490–2492.
Osgood, W. H. 1909. Revision of the mice of the American genus Peromyscus. North American Fauna 28:1–285.
Platt, R. N. II., et al. 2015. What is Peromyscus? Evidence from nuclear and mitochondrial DNA sequences suggests the need for a new classification. Journal of Mammalogy 96:708–719.
Rambaut, A., et al. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67:901–904.
Riddle, B., et al. 2000. Phylogeography and Systematics of the Peromyscus eremicus species group and the historical biogeography of North American Warm Regional deserts. Molecular Phylogenetics and Evolution 17:145–160.
Rohland, N., and D. Reich. 2012. Cost-effective, high-throughput DNA sequencing libraries for multiplexed target capture. Genome Research 22:939–946.
Ronquist, F., and J. P. Huelsenbeck. 2003. MRBAYES 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574.
Roycroft, E., et al. 2021. Museum genomics reveals the rapid decline and extinction of Australian rodents since European settlement. Proceedings of the National Academy of Sciences 118:e2021390118.
Roycroft, E., et al. 2022. Sequence capture from historical museum specimens: maximizing value for population and phylogenomic studies. Frontiers in Ecology and Evolution 10:931644.
Sacks, B. N., et al. 2021. Pleistocene origins, western ghost lineages, and the emerging phylogeographic history of the red wolf and coyote. Molecular Ecology 30:4292-4304.
Schimidly, D. J., et al. 1985. Systematics and notes on the biology of Peromyscus hooperi. Occasional Papers, Museum of Texas Tech University 97:1–40.
Schmieder, R., and R. Edwards. 2011. Quality control and preprocessing of metagenomic datasets. Bioinformatics 27:863–864.
Secretaría de Medio Ambiente y Recursos Naturales. 2010. Norma Oficial Mexicana NOM-059-SEMARNAT-2010, Protección ambiental–Especies nativas de México de flora y fauna silvestres–Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio–Lista de especies en riesgo. Diario Oficial de la Federación. México. 30 de diciembre de 2010.
Sawyer, Y. E., et al. 2017. Diversification of deermice (Rodentia: genus Peromyscus) at their north- western range limit: genetic consequences of refugial and island isolation. Journal of Biogeography 44:1572-1585.
Sayyari, E., and S. Mirarab. 2016. Fast coalescent-based computation of local branch support from quartet frequencies. Molecular Biology and Evolution 33:1654–1668.
Stamatakis, A. 2014. RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313.
Steppan, S., and J. J. Schenk. 2017. Muroid rodent phylogenetics: 900-species tree reveals increasing diversification rates. PLoS ONE 12:e0183070.
Sullivan, K. A. M., et al. 2017. Whole mitochondrial genomes provide increased resolution and indicate paraphyly in deer mice. BMC Zoology 2:11.
Tavares, V.C., et al. 2022. Historical DNA data of rare Yellow-eared bats Vampyressa Thomas, 1900 (Chiroptera, Phyllostomidae) clarifies phylogeny and species boundaries within the genus. Systematics and Biodiversity 20:1.
Wright, E. A., et al. 2020. Evidence from mitochondrial DNA sequences suggest a recent origin for Peromyscus truei comanche. Occasional Papers Texas Tech University Museum 367:1–19.
Zhang C., et al. 2018. ASTRAL-III: Polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinformatics 19:15–30.
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.
