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Physical and ecological isolation contribute to maintain genetic differentiation between fire salamander subspecies

Abstract

Landscape features shape patterns of gene flow among populations, ultimately determining where taxa lay along the continuum between panmixia to complete reproductive isolation. Gene flow can be restricted, leading to population differentiation in two non-exclusive ways: “physical isolation”, in which geographic distance in combination with the landscape features restricts movement of individuals promoting genetic drift, and “ecological isolation”, in which adaptive mechanisms constrain gene flow between different environments via divergent natural selection. In central Iberia, two fire salamander subspecies occur in parapatry across elevation gradients along the Iberian Central System mountains, while in the adjacent Montes de Toledo Region only one of them occurs. By integrating population and landscape genetic analyses, we show a ubiquitous role of physical isolation between and within mountain ranges, with unsuitable landscapes increasing differentiation between populations. However, across the Iberian Central System, we found strong support for a significant contribution of ecological isolation, with low genetic differentiation in environmentally homogeneous areas, but high differentiation across sharp transitions in precipitation seasonality. These patterns are consistent with a significant contribution of ecological isolation in restricting gene flow among subspecies. Overall, our results suggest that ecological divergence contributes to reduce genetic admixture, creating an opportunity for lineages to follow distinct evolutionary trajectories.

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Fig. 1: Sampling localities represented by dots (size refers to number of individuals genotyped for microsatellites, see Table 1 for details).
Fig. 2: Population structure and allelic richness.
Fig. 3: Genetic and ecological differentiation.

Data availability

Individual genotypes have been deposited in Dryad (https://doi.org/10.5061/dryad.rjdfn2z97).

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Acknowledgements

We thank A. Álvarez, M.J. Fernández Benéitez, D. Fernández Ortín, R. Finat, C. Grande, J. Gutiérrez Rodríguez, P. Hernández Sastre, E. Jockusch, J.R. Mayor, M. Modrell, E. Recuero, G. Sánchez Montes, A. Sánchez Vialas, J.A. Saz, and F. Smith for help in collecting samples, and A. Lourenço and J. Gutiérrez Rodríguez for help with lab work. We appreciate the help of I. Rey and B. Álvarez (Tissue and DNA collection, MNCN-CSIC) for access to samples under their care. The Associate Editor R. Faria, W. Babik and three anonymous reviewers provided constructive comments that contributed to improve the manuscript. GV-A was supported by FCT – Foundation for Science and Technology (CEECIND/00937/2018). This research was supported by the European Science Foundation (Frontiers of Speciation Research, Exchange grant 3318), and by the European Commission (Synthesys grant ES-TAF-1486), granted to RJP. Partial funds were additionally provided by grants EVOVIV: PTDC/BIA-EVF/3036/2012 (FCT, Portugal) to GV-A, and CGL2017-83131-P (FEDER/Ministerio de Ciencia, Innovación y Universidades–Agencia Estatal de Investigación, Spain) to IMS.

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Antunes, B., Velo-Antón, G., Buckley, D. et al. Physical and ecological isolation contribute to maintain genetic differentiation between fire salamander subspecies. Heredity 126, 776–789 (2021). https://doi.org/10.1038/s41437-021-00405-0

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