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Conservation genetics of two critically endangered island dwarf carnivores

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Abstract

Genetic diversity is crucial for conservation biology and for understanding evolutionary processes. Oceanic islands harbor a unique biota and high endemism, with populations frequently facing detrimental genetic processes (e.g. drift, bottlenecks). Human activities like habitat transformation further increase extinction risk of insular biota. Mammals comprise the most endangered group among insular fauna. Our aim was to evaluate the genetic and evolutionary patterns of two critically endangered dwarf carnivores from Cozumel Island, the pygmy raccoon (Procyon pygmaeus) and the dwarf coati (Nasua nelsoni), at both historical and contemporary evolutionary scales. We also reviewed their genetic relationships with their mainland counterparts (P. lotor, N. narica), not intended to describe their phylogeny but to ascertain their endemism. Our mitochondrial results support that both Cozumel carnivores are divergent from continental populations, strengthening their endemic status. Both species showed moderate levels of nuclear genetic diversity that were, as expected for island populations, lower in comparison with their mainland congeneric species; they also exhibited significantly low population sizes. We documented historical and contemporary bottleneck signals for P. pygmaeus, whereas N. nelsoni may be suffering the initial stages of a bottleneck not yet fully manifested. The pygmy raccoon is structured into two isolated genetic clusters likely due to interactions with humans on the north of the island, where most potential for disease transmission and health problems exist. We also add evidence about the introduction of the mainland species into the island, risking genetic introgression and hybridization. We discuss specific conservation measures that should include our genetic information, directed to the long-term viability of these endemic carnivores.

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Data availability

All data generated or analysed during this study are included in this published article and its supplementary materials files. Cytochrome b sequences are in GenBank (Accession numbers of unique haplotypes for Procyon lotor: OK087548-OK087550; Procyon pygmaeus: OK087551; Nasua narica: OK087552-OK087556; Nasua nelsoni: OK087557-OK087562; Table S1).

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Acknowledgements

We are grateful with all those that helped during fieldwork, K. McFadden†, D. García-Vasco, M. Copa-Álvaro, J.C. Martínez, H. Mena, C. Rodríguez, S. Lara, and with A. Morales, S. Pérez-Consuegra and G. Pacheco-Sierra for molecular advice. We deeply thank C. González-Baca, H. Ayuntamiento de Cozumel, Comisión de Agua Potable y Alcantarillado, Comisión Nacional de Áreas Naturales Protegidas, Cozumel Country Club, Durrell Wildlife Conservation Trust, Fundación de Parques y Museos de Cozumel, International Fund for Animal Welfare, Junta Coordinadora Empresarial de Cozumel, Sociedad Humanitaria de Cozumel, and other institutions, colleagues and friends in Cozumel for all their support. Two anonymous reviewers made key comments that truly helped us. AFM acknowledges that this paper was a part of his Master’s thesis in the Posgrado en Ciencias Biológicas de la Universidad Nacional Autónoma de México. We dedicate this manuscript to the memory of Miguel A. Martínez Morales, colleague and friend that worked intensively for the knowledge and conservation of the biota of Cozumel, and who will be greatly missed.

Funding

Funding for this research was partially provided by Comisión Nacional de Áreas Naturales Protegidas (Programa de Recuperación de Especies en Riesgo, PROCER-CONANP PROCER 2013 and 2014) granted to Miguel Martínez Morales†. Research grants were received by ADC from Consejo Nacional de Ciencia y Tecnología (CONACyT; grant #33635-V), Fondo Sectorial de Investigación Ambiental (Semarnat-2002-C01-0571), and Comisión Nacional sobre el Conocimiento y Uso de la Biodiversidad (Conabio project LI028), DVG from UC NEXUS-CONACYT Collaborative Research Grants (CN-12-627), and EVD from CONACyT (No. 101861) and Papiit (IN217910). AFM had a scholarship and financial support provided by CONACyT (CVU 440854/Reg. becario 271066).

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Authors and Affiliations

  1. Departamento de Ecología de la Biodiversidad, Instituto de Ecología, Universidad Nacional Autónoma de México, Coyoacán, 04510, Mexico City, Mexico

    Alejandro Flores-Manzanero & Ella Vázquez-Domínguez

  2. Centro de Investigación en Biodiversidad y Conservación, Universidad Autónoma del Estado de Morelos, 62209, Cuernavaca, Morelos, Mexico

    David Valenzuela-Galván

  3. SACBÉ – Servicios Ambientales, Conservación Biológica y Educación A.C., Coyoacán, 04010, Mexico City, Mexico

    Alfredo D. Cuarón

  4. Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Coyoacán, 04510, Mexico City, Mexico

    Alejandro Flores-Manzanero

Authors
  1. Alejandro Flores-Manzanero
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  2. David Valenzuela-Galván
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  3. Alfredo D. Cuarón
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  4. Ella Vázquez-Domínguez
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Contributions

All authors contributed to the study conception and design. A. Flores-Manzanero, D. Valenzuela-Galván, and A.D. Cuarón performed field work. A. Flores-Manzanero and E. Vázquez-Domínguez performed analyses and interpretation of results. All authors wrote the manuscript and approved submission.

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Correspondence to Ella Vázquez-Domínguez.

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All procedures were conducted according to the American Society of Mammalogists guidelines for use of wild mammal species (ASM; Sikes et al. 2016).

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Flores-Manzanero, A., Valenzuela-Galván, D., Cuarón, A.D. et al. Conservation genetics of two critically endangered island dwarf carnivores. Conserv Genet 23, 35–49 (2022). https://doi.org/10.1007/s10592-021-01401-x

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