Allele surfing shaped the genetic structure of the European pond turtle via colonization and population expansion across the Iberian Peninsula from Africa

• Published in: Journal of biogeography 2018-09, Vol.45 (9), p.2202-2215
• Main Authors: Pereira, Paulo, Teixeira, José, Velo-Antón, Guillermo
• Format: Article
• Language: English
• Subjects: allele surfing; Alleles; Association analysis; Barriers; Colonization; Empirical analysis; Emys orbicularis; Environmental organizations; Frequency analysis; Gene flow; Gene frequency; Genetic analysis; Genetic diversity; Genetic drift; Genetic structure; Genotype & phenotype; Habitat loss; isolation by distance; Loci; Natural populations; Natural selection; Permutations; Ponds; Population; Population genetics; Population growth; Population studies; Populations; range expansions; Range extension; RESEARCH PAPER; Signatures; Sliding; Test procedures
• ISSN: 0305-0270; 1365-2699
• DOI: 10.1111/jbi.13412

Aim: Allele surfing remains poorly investigated in empirical studies due to a lack of explicit methods to detect it in natural populations. Here, we introduce a spatially explicit, sliding-window method to test hypotheses on how range expansions and geographic barriers impact neutral genetic structure using allele frequency data. We then use this approach to study the Ibero-Moroccan lineage of the European pond turtle, Emys orbicularis occidentalis, which recolonized the Iberian Peninsula from Africa. Location: Iberian Peninsula, Morocco. Methods: We generated a dataset of 453 genotyped individuals from 21 populations from throughout the E. o. occidentalis distribution at seven microsatellite loci. The microsatellite data were used to evaluate spatial patterns of genetic diversity and structure, as well as recent gene flow between populations. Using a spatially explicit, sliding-window approach, linear models and permutation tests, we tested for signals of allele surfing throughout the Iberian populations, including barriers to gene flow that may enhance the effect of founder events typical of range expansions. Finally, we tested for signatures of adaptation on identified surfing alleles using environmental association analysis. Results: Our study identified signatures of allele surfing throughout the range of Iberian populations. We did not find evidence that any of the loci studied are under natural selection. We therefore concluded that allele surfing has had a significant impact on genetic structure observed in E. o. occidentalis. Population isolation and fragmentation, due to habitat loss, further contribute to the present genetic differentiation between populations. Main conclusion: The sliding-window method proposed herein can help to identify alleles that underwent allele surfing at the front of range expansions. This study also highlights the role of genetic drift and geographic barriers in shaping the species' genetic structure following population range expansions. Finally, we stress the importance of evaluating the existence of allele surfing processes in biogeographic and population genetic studies, relying on allele frequency analysis, for a better interpretation of contemporary patterns of intraspecific genetic structure.