Molecular, morphometric, and spatial data analyses provide new insights into the evolutionary history of the Peromyscus boylii species complex (Rodentia: Cricetidae) in the mountains of Mexico

Abstract

Peromyscus is the most speciose genus in America, which occupies almost every terrestrial habitat type. However, its taxonomy and evolutionary relationships remain unsolved in several species, one species group with these issues is the P. boylii complex. This complex consists of 11 species (P. beatae, P. boylii, P. carletoni, P. ensinki, P. greenbaumi, P. kilpatricki, P. levipes, P. madrensis, P. schmidlyi, P. simulus, and P. stephani) largely distributed in Mexico and has been taxonomically studied during the last 40 years, resulting in the description of new species, several of them from the mountains of central Mexico. In this study, we aimed to integrate molecular, morphometric, and spatial data analysis approaches to inquire into the phylogenetic relationships. To clarify the taxonomic status of the P. boylii complex, particularly for the species distributed in the central Mexican highlands where the taxonomic uncertainty is high. We performed phylogenetic and divergence time analyses based on four molecular markers for all species within the complex, we explored cranium shape and size variation in 146 individuals of continental species (P. madrensis and P. stephani excluded) using geometric morphometrics. Also, we evaluated environmental differentiation and ecological niche modeling analyses of three species endemic to the central Mexican highlands to retrieve evidence on their evolutionary history. Our results recovered one well-supported clade including all mountainous species, in which P. schmidlyi was sister to the clade composed of P. greenbaumi and P. ensinki, which diverged during the late Pleistocene. The novel morphological data allowed a better differentiation of all continental species. The discovery of new specimens for P. greenbaumi and P. ensinki improved their taxonomic knowledge, as well as delimiting their habitat and distribution, showing substantial environmental divergence with low overlapped geographical distributions; P. schmidlyi restricted to the Sierra Madre Occidental, P. ensinki to the central-west Trans-Mexican Volcanic Belt, and P. greenbaumi to the center of the Sierra Madre del Sur. We discuss the biogeographic history of these three lineages and the role of the late Pleistocene climatic oscillations on their diversification.

Key words:

• environmental niche divergence
• geometric morphometrics
• molecular phylogenetics
• Neotominae
• Pleistocene
• Rodent
• Sierra Madre del Sur
• Sierra Madre Occidental
• Trans-Mexican Volcanic Belt

Acknowledgements

This work was supported by the Consejo Nacional de Ciencia y Tecnología México under grant (346631 to MALT). To curators and associated staff for their patience and help in accessing museum specimens, associated data, tissue samples: Fernando A. Cervantes and Yolanda Hortelano Moncada at the Colección Nacional de Mamíferos; Elizabeth Arellano Arenas and Francisco Xavier González Cózatl at the Colección de Mamíferos of the Universidad Autónoma de Morelos; José Ramírez Pulido and Noé González Ruiz at the Colección de Mamíferos of the Universidad Autónoma Metropolitana, Unidad Iztapalapa. Celia López González, and Diego F. García Mendoza from the mammal collection of the Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional Unidad Durango, Instituto Politécnico Nacional, provided occurrence data for Peromyscus schmidlyi. Andrea Ballen Guapacha drew the schematic cranium illustrations. Janet Nolasco provides logistic support for laboratory work, and Cristina Bárcenas Pazos helped us in sequencing DNA samples at the Instituto de Ecología AC. Celia López-González, Francisco Ornelas, Francisco González-Cózatl, Andrés Lira, Ulyses Pardiñas, and one anonymous reviewer provided comments that improved the manuscript.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Supplemental material

Supplemental material for this article can be accessed here: https://dx.doi.org/10.1080/14772000.2022.2127966.

Associate Editor: Dr Susan Tsang