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Open Access Highly Accessed Research article

Asymmetric reproductive isolation between terminal forms of the salamander ring species Ensatina eschscholtzii revealed by fine-scale genetic analysis of a hybrid zone

Thomas J Devitt13*, Stuart JE Baird2 and Craig Moritz1

Author Affiliations

1 Museum of Vertebrate Zoology and Department of Integrative Biology, 3101 Valley Life Sciences Building, University of California, Berkeley, CA, USA 94720-3160

2 CIBIO, University of Porto, Campus Agrário de Vairão, Rua Padre Armando Quintas 7, 4485-661 Vairão, Portugal

3 Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Circuito exterior s/n, Ciudad Universitaria, Copilco, Coyoacán, A.P. 70-153/70-233 México, Distrito Federal. C.P. 04510

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BMC Evolutionary Biology 2011, 11:245  doi:10.1186/1471-2148-11-245

Published: 22 August 2011

Abstract

Background

Ring species, exemplified by salamanders of the Ensatina eschscholtzii complex, represent a special window into the speciation process because they allow the history of species formation to be traced back in time through the geographically differentiated forms connecting the two terminal forms of the ring. Of particular interest is the nature and extent of reproductive isolation between the geographically terminal forms, in this case E. e. eschscholtzii and E. e. klauberi. Previous studies have documented infrequent hybridization at the end of the ring. Here, we report the first fine-scale genetic analysis of a hybrid zone between the terminal forms in southern California using individual-based Bayesian analyses of multilocus genetic data to estimate levels and direction of hybridization and maximum-likelihood analysis of linkage disequilibrium and cline shape to make inferences about migration and selection in the hybrid zone.

Results

The center of the hybrid zone has a high proportion of hybrids, about half of which were classified as F1s. Clines are narrow with respect to dispersal, and there are significant deviations from Hardy-Weinberg equilibrium as well as nonrandom associations (linkage disequilibria) between alleles characteristic of each parental type. There is cytonuclear discordance, both in terms of introgression and the geographic position of mitochondrial versus nuclear clines. Genetic disequilibrium is concentrated on the eschscholtzii side of the zone. Nearly all hybrids possess klauberi mtDNA, indicating that most hybrids are formed from female klauberi mating with male eschscholtzii or male hybrids (but not vice versa).

Conclusions

Our results are consistent with a tension zone trapped at an ecotone, with gene combinations characteristic of klauberi showing up on the eschscholtzii side of the zone due to asymmetric hybridization. We suggest that the observed asymmetry is best explained by increased discriminatory power of eschscholtzii females, or asymmetric postzygotic isolation. The relatively high frequency of hybrids, particularly F1s, contrasts with other contacts between the terminal forms, and with other contacts between other divergent Ensatina lineages, highlighting the diverse outcomes of secondary contact within a single species complex.