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Mitogenomic phylogenetics and population genetics of several taxa of agouties (Dasyprocta sp., Dasyproctidae, Rodentia): molecular nonexistence of some claimed endemic taxa

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Abstract

Some neotropical rodents are of special interest because they are an important source of animal protein for human indigenous populations throughout Latin America. This is the case of the genus Dasyprocta (agouties). However, we still do not know how many species, taxa, or lineages are within Dasyprocta. To address this issue, we analyzed the complete mitogenomes of 93 specimens in addition to three mitochondrial genes of 128 specimens of Dasyprocta belonging to six supposed species (D. fuliginosa, D. punctata, D. leporina, D. kalinowski, D. ruatanica, and D. azarae). The phylogenetic results indicated five different lineages within D. fuliginosa, with two being polyphyletic (one more related to D. leporina and another more related to D. punctata). D. kalinowski, a species endemic to Peru, was un-differentiable from one of these D. fuliginosa lineages. D. azarae was related with some of the lineages of D. fuliginosa. Within D. leporina, two significant lineages were found (in central Atlantic Brazil and on the Caribbean islands of Trinidad and Tobago). Within D. punctata, three lineages were detected, one in Central America (central and northern), including D. ruatanica, a supposed endemic species on Roatan Island, Honduras, another in central and southern Panama, and another in trans-Andean and Pacific Colombia and Ecuador. Some of the lineages of D. fuliginosa from the western Amazon yielded the most ancestral haplotypes (around 7 million years ago, MYA, Late Miocene). In contrast, haplotypes of a lineage of D. punctata and those of a lineage of D. leporina (Trinidad and Tobago) were the most derived (around 0.2–0.3 MYA, Pleistocene). Other population genetic results showed that all groups or lineages presented elevated levels of genetic diversity, with the exception D. leporina in Trinidad and Tobago. Their lower genetic diversity is probably related to founder effect during the colonization of the Caribbean island, due to a bottleneck. Some of these Dasyprocta taxa showed some population expansions during the Pleistocene, but all of the lineages experienced some population decrease during the last 10,000–20,000 years. Note that some lineages showed a small population increase in the last few centuries. The spatial genetic structure was highly developed throughout the Neotropics for Dasyprocta. According to this study, (1) coat color (routinely used in the systematics of this rodent) is not valuable from a phylogenetic and systematics perspective and (2) two supposedly endemic species (D. kalinowski and D. ruatanica) were not full species. These results are of vital importance for the biological conservation of the different taxa and lineages of this rodent.

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Acknowledgements

Thanks to Dr. Diana Alvarez, Pablo Escobar-Armel, Nicolás Lichilín, and Luisa Fernanda Castellanos-Mora for their respective help in obtaining Dasyprocta samples during the last 20 years. Thanks to the Ministerio del Ambiente Ecuatoriano (MAE) in Santo Domingo de Tsáchilas and in Coca, and INABIO (Ecuador), to the Instituto von Humboldt (Colombia), to the Peruvian Ministry of Environment, PRODUCE (Dirección Nacional de Extracción y Procesamiento Pesquero), Consejo Nacional del Ambiente and the Instituto Nacional de Recursos Naturales (INRENA) from Peru, to the Colección Boliviana de Fauna (Dr. Julieta Vargas), and to CITES Bolivia for their role in facilitating the obtainment of the collection permits in Ecuador, Colombia, Peru and Bolivia. The first author also thank the many people of diverse Indian tribes in Ecuador (Kichwa, Huaorani, Shuar and Achuar), in Colombia (Jaguas, Ticunas, Huitoto, Cocama, Tucano, Nonuya, Yuri and Yucuna), in Peru (Bora, Ocaina, Shipigo-Comibo, Capanahua, Angoteros, Orejón, Cocama, Kishuarana and Alamas), Bolivia (Sirionó, Canichana, Cayubaba and Chacobo), and to diverse Mayan communities and peasants from Guatemala, Honduras, and Panama for their assistance in obtaining samples of Dasyprocta.

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Authors and Affiliations

  1. Laboratorio de Genética de Poblaciones Molecular-Biología Evolutiva, Departamento de Biología, Facultad de Ciencias, Pontificia Universidad Javeriana, Cra 7A, No. 43-82, Bogotá, DC, Colombia

    Manuel Ruiz-García, Ana María Cáceres & Kelly Luengas-Villamil

  2. Instituto de Ecología, Universidad Mayor de San Andrés, Calle 27 Cota Cota, Campus Universitario, La Paz, Bolivia

    Enzo Aliaga-Rossel

  3. Universidad Católica de Santa María, Urb. San José S/N, Umacollo, Arequipa, Peru

    Horacio Zeballos

  4. Faculty of Food and Agriculture, The University of the West Indies, St. Augustine Campus, St. Augustine, Trinidad and Tobago

    Michele D. Singh

  5. Math, Science and Technology Department, University of Minnesota Crookston, 2900 University Ave, Crookston, MN, 56716, USA

    Joseph Mark Shostell

Authors
  1. Manuel Ruiz-García
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  2. Ana María Cáceres
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  3. Kelly Luengas-Villamil
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  4. Enzo Aliaga-Rossel
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  5. Horacio Zeballos
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  6. Michele D. Singh
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  7. Joseph Mark Shostell
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Contributions

M. R. G. designed and obtained a large proportion of the samples for the study. E. A. R., H. Z., and M. D. S. helped to obtain some relevant samples in Bolivia, southern Peru, and Trinidad Island, respectively. M. R. G. and J. M. S. supervised the molecular analyses. A.M.C. and K.L.V performed the laboratory procedures. M. R. G. performed the statistical analyses and wrote the manuscript with input from the other authors. M. R. G. submitted the sequences to GenBank. E. A. R., H. Z, M. D. S., A. M. C., K. L. V., and J. M. S. revised the manuscript. All authors read and approved the final version of the manuscript.

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Correspondence to Manuel Ruiz-García.

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Ruiz-García, M., Cáceres, A.M., Luengas-Villamil, K. et al. Mitogenomic phylogenetics and population genetics of several taxa of agouties (Dasyprocta sp., Dasyproctidae, Rodentia): molecular nonexistence of some claimed endemic taxa. Mamm Res 67, 367–397 (2022). https://doi.org/10.1007/s13364-022-00626-6

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