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Using Ultraconserved Elements to Unravel Lagomorph Phylogenetic Relationships

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Abstract

Lagomorpha (lagomorphs), the order of mammals including pikas, hares, and rabbits, is distributed on all continents. The order currently is hypothesized to comprise 12 genera and 108 species, split into two families: Ochotonidae (pikas) and Leporidae (rabbits and hares). Molecular and morphological attempts have been undertaken to resolve the phylogeny of lagomorphs, although chronological relationships are still to be established. The aim of this research was to unravel lagomorph phylogeny using ultraconserved elements. We focused on Romerolagus, in light of its largely unknown phylogenetic relationships and sparse fossil record, to assess times of divergence for the genus. We obtained samples from at least one species in each of 11 genera (except Caprolagus) comprising the order and captured and sequenced ultraconserved elements (UCEs). A Maximum-Likelihood phylogenetic analysis was carried out on the 4,195 loci captured, resulting in 59,112 informative sites. We further used BEAST2 v2.6.3 on the CIPRES computing cluster to estimate the timing of cladogenesis in lagomorph evolution. Our results confirm that lagomorphs and rodents split about 65 million years ago. The former further split into its constituent families, Leporidae and Ochotonidae, about 60 million years ago. Pronolagus rupestris and Nesolagus timminsi were retrieved as basal sister taxa; the most recent common ancestor of that clade and remaining leporids was estimated to have existed about 47 million years ago. Romerolagus diazi is sister to remaining Leporidae excluding Pronolagus and Nesolagus, a topology that generally matches previously published phylogenies, although our results suggest a most recent common ancestor of Romerolagus and remaining ingroup leporids at ca. 4.8 Ma (95% highest posterior density [HPD] interval: 5.9 – 3.8 Ma), with an internal diversification in the Middle to Late Pleistocene (0.9 Ma; 95% HPD 1.8 – 0.2 Ma). Our final results yielded a robust phylogeny with high support values for every clade of the order Lagomorpha and unraveled previously unresolved phylogenetic relationships. In addition, we further conclude that the method we used, UCEs, may serve to complete the entire phylogeny of mammals by using existing museum specimens.

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Fig. 1
Fig. 2

adapted from Ruedas et al. (2019). a. Romerolagus diazi, USNM 57949 (holotype of R. nelsoni Merriam 1896); b. Nesolagus netscheri, MNH (London) 1921.1.18.1 (left, reversed); c. Nesolagus timminsi, MNH (London) 1997.396 (left, reversed). Note the double layer of enamel on the anterior lobe of N. netscheri, stretching from immediately lingual of the central angle to the caudal aspect of the protoflexid. The condition of having two layers of enamel forming a tooth facet in Lagomorpha previously was reported once only (see Ruedas et al. 2019:fig. 6), on the caudal face (rostral facing aspect) of the hypoflexid of the holotype of Sylvilagus incitatus (Bangs, 1901) (Harvard Museum of Comparative Zoology Bangs Collection no. 8441)

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All sequences are in process of submission to GenBank.

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Acknowledgments

The present research was submitted in partial fulfilment to obtain the grade of Masters in Biological Sciences of the first author. We thank the “Posgrado en Ciencias Biológicas” from the “Universidad Nacional Autónoma de México (Programa 134, Entidad 97, Plan 4085, Orientación 4)”. We acknowledge the support from, and the samples of Lepus flavigularis donated by Dra. Consuelo Lorenzo Monterrubio and the staff of the Mammal Collection from ECOSUR ; the “Dirección General de Zoológicos y Conservación de la Fauna Silvestre”, “Dirección de Operación Científica y Técnica” and “Chapultepec Zoo” for samples of Romerolagus diazi; the Zoology Museum “Alfonso L. Herrera” of the Faculty of Sciences—UNAM (MZFC-M) for R. diazi, Sylvilagus floridanus, Sylvilagus cunicularius, and Neotomodon alstoni; the Surgery Office from the School of Medicine – UNAM for Oryctolagus cuniculus; the Museum of Comparative Zoology (MCZ-CRYO, Mammalogy) of Harvard University for Bunolagus monticularis and Caprolagus [= Lepus] sinensis flaviventris; the Mammal Division of the University of Michigan Museum of Zoology for the donation of the Pentalagus furnessi sample; the Mammal Collection of the University of New Mexico – Museum of Southwestern Biology, for Brachylagus idahoensis; the Department of Mammalogy of the American Museum of Natural History for Nesolagus timminsi; the Division of Mammals at The Field Museum of Natural History for Ochotona princeps lasalensis, Caprolagus hispidus, and especially Pronolagus rupestris nyikae and Poelagus marjorita, specimens of which were collected by J. C. Kerbis Peterhans. Special thanks to A. W. Ferguson and K. Feldheim for their support in the process of collecting samples and lab work at the Pritzker Laboratory for Molecular Systematics and Evolution. Portions of this work were undertaken under the auspices of NSF grant DEB–0616305 to L.A. Ruedas, who also thanks D. Lunde and A. L. Gardner (USNM) and R. Portela Míguez (MNH London) for access to specimens whose dentitions were illustrated. Support to conclude this manuscript came from UNAM-DGAPA-PAPIIT (Project IN105721). N. Arkhanhelskaya provided a through English editorial review of the present version.

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Authors and Affiliations

  1. Posgrado en Ciencias Biológicas, UNAM, Av. Ciudad Universitaria 3000, C.P. 04510, Coyoacán, Ciudad de México, México

    Estefania Cano-Sánchez

  2. Centro Universitario de Ciencias Exactas e Ingenierías, Universidad de Guadalajara, Blvd. Marcelino García Barragán No. 1421, esq. Calzada Olímpica, Z. C. 44430, Guadalajara, Jalisco, México

    Flor Rodríguez-Gómez

  3. Department of Biology and Museum of Natural History, Science Research and Teaching Center, Portland State University, Portland, OR, 97207–0751, USA

    Luis A. Ruedas

  4. Escuela Nacional de Estudios Superiores Unidad Morelia, UNAM, Antigua Carretera a Pátzcuaro No. 8701, Col. Ex Hacienda de San José de la Huerta, Z. C. 58190, Morelia, Michoacán, México

    Ken Oyama

  5. Departamento de Biología Evolutiva, Museo de Zoología “Alfonso L. Herrera”, Facultad de Ciencias, UNAM, C. U., Coyoacán, Z. C. 04510, Ciudad de México, México

    Livia León-Paniagua

  6. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, Liga Periférico-Insurgentes Sur No. 4903, Parques del Pedregal, Z. C. 14010, Tlalpan, Ciudad de México, Mexico

    Alicia Mastretta-Yanes

  7. Centro de Investigaciones en Geografía Ambiental, UNAM, Antigua Carretera a Pátzcuaro No. 8701, Col. Ex Hacienda de San José de la Huerta, Z. C. 58190, Morelia, Michoacán, México

    Estefania Cano-Sánchez & Alejandro Velazquez

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  1. Estefania Cano-Sánchez
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  2. Flor Rodríguez-Gómez
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Contributions

Estefania Cano-Sánchez: Conceptualization, Methodology, Software, Formal analysis, Investigation, Data Curation, Writing-Original Draft, Visualization; Flor Rodríguez-Gómez: Software, Validation, Formal analysis, Writing-Review & Editing, Visualization, Supervision; Ken Oyama: Conceptualization, Writing-Review & Editing, Funding acquisition; Livia León-Paniagua: Conceptualization, Resources, Writing-Review & Editing, Supervision; Luis A. Ruedas: Re-scope of the contribution, data analyses, outreach and Writing-Review & Editing; Alicia Mastretta-Yanes: Conceptualization Writing-Review & Editing; Alejandro Velazquez: Conceptualization, Investigation, Funding acquisition, Writing-Review & Editing, Supervision, Project administration.

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Correspondence to Alejandro Velazquez.

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Cano-Sánchez, E., Rodríguez-Gómez, F., Ruedas, L.A. et al. Using Ultraconserved Elements to Unravel Lagomorph Phylogenetic Relationships. J Mammal Evol 29, 395–411 (2022). https://doi.org/10.1007/s10914-021-09595-0

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