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Idiosyncratic responses to drivers of genetic differentiation in the complex landscapes of Isthmian Central America

Abstract

Isthmian Central America (ICA) is one of the most biodiverse regions in the world, hosting an exceptionally high number of species per unit area. ICA was formed <25 million years ago and, consequently, its biotic assemblage is relatively young and derived from both colonization and in situ diversification. Despite intensive taxonomic work on the local fauna, the potential forces driving genetic divergences and ultimately speciation in ICA remain poorly studied. Here, we used a landscape genetics approach to test whether isolation by distance, topography, habitat suitability, or environment drive the genetic diversity of the regional frog assemblage. To this end, we combined data on landscape features and mitochondrial DNA sequence variation for nine codistributed amphibian species with disparate life histories. In five species, we found that at least one of the factors tested explained patterns of genetic divergence. However, rather than finding a general pattern, our results revealed idiosyncratic responses to historical and ecological processes, indicating that intrinsic life-history characteristics may determine the effect of different drivers of isolation on genetic divergence in ICA. Our work also suggests that the convergence of several factors promoting isolation among populations over a heterogeneous landscape might maximize genetic differentiation, despite short geographical distances. In conclusion, abiotic factors and geographical features have differentially affected the genetic diversity across the regional frog assemblage. Much more complex models (i.e., considering multiple drivers), beyond simple vicariance of Caribbean and Pacific lineages, are needed to better understand the evolutionary history of ICA’s diverse biotas.

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Fig. 1: Map of the study region including the major topographic features of Isthmian Central America (ICA) and place names mentioned in the text.
Fig. 2: Phylogeographic structure within each focal species mapped over a topographic map of the study area.
Fig. 3: Generalized dissimilarity model-fitted I splines for the variables that contributed more in explaining genetic differentiation based on the 16S fragment.

Data availability

Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.2jm63xsn0.

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Acknowledgements

We thank Federico Bolaños (UCR) for permission and access to the samples sequenced for this study and Sandra “Vicky” Flechas for her patient collaboration during lab procedures. Javier Guevara and the Sistema Nacional de Áreas de Conservación de Costa Rica provided collecting permits that ended up in most of the samples here analyzed. We wish to acknowledge funding from the Smithsonian Institution’s DNA Barcode Network (FY11 Award cycle to E. Bermingham) and the use of facilities at Naos Marine and Molecular Labs, Smithsonian Tropical Research Institute, Panama. AG-R is currently supported by a postdoctoral fellowship from Dirección General de Asuntos del Personal Académico (DGAPA) at Instituto de Biología, Universidad Nacional Autónoma de México. AG-R also acknowledges Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brazil (CAPES) for the financial support during his PhD and Gerardo Chaves (MZUCR) for his teachings during innumerous field trips, as well as for the constant discussion on the herpetology of Central America. AJC was supported by Research Program INV-2017-51-1432 from the School of Sciences, Universidad de los Andes. Víctor Acosta and Brian Gratwicke kindly provided the photos used in Fig. 3. Fabricio Villalobos, Diogo Provete, Sergio Lima, Erick Arias-Piedra, and three anonymous reviewers provided valuable feedback to improve the quality of this paper.

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García-Rodríguez, A., Guarnizo, C.E., Crawford, A.J. et al. Idiosyncratic responses to drivers of genetic differentiation in the complex landscapes of Isthmian Central America. Heredity 126, 251–265 (2021). https://doi.org/10.1038/s41437-020-00376-8

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