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

Abstract

BackgroundRing 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.ResultsThe 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).ConclusionsOur 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.

Evolution and stability of ring species

“…Although natural and/or sexual selection appear to be important for greenish warblers' traits (11,16,17) and those of other potential ring species (13,18,(25)(26)(27)(28)(29), our results show that their role in the emergence of reproductive isolation and maintenance of ring species (as suggested in ref . 11) is not yet well understood.…”

Wherefore and Whither the Ring Species?

“…An ideal ring species would display complete reproductive isolation. In reality, small amounts of hybridization between the terminal forms are tolerated (Pereira and Wake, 2009;Devitt et al, 2011;Alcaide et al, 2014), which is consistent with how species are commonly diagnosed under the biological species concept (Coyne and Orr, 2004).…”

“…pervasive in the mid-ring contact between xanthoptica and eschscholtzii (Brown, 1974;Wake et al, 1989;Alexandrino et al, 2005;Pereira and Wake, 2009) than it is in the terminal contact between klauberi and eschscholtzii (Brown, 1974;Devitt et al, 2011). Both regions of contact involve what would be considered species-level entities by most criteria, except an extreme version of the biological species concept that does not allow for any interbreeding at all.…”

“…In the mountains of southern California the unblotched subspecies eschscholtzii and the blotched subspecies klauberi are locally sympatric (Stebbins, 1949(Stebbins, , 1957Brown and Stebbins, 1964;Brown, 1974;. A recent detailed study of one of several areas of contact in southern California (Palomar Mountain, San Diego Co.) described a hybrid zone located along an ecotone, with pure parentals and F1s dominating in the region of overlap (Devitt et al, 2011). In a nearby site in the Cuyamaca Mountains (the southernmost known area of contact) no evidence of present or past hybridization is evident, and the two morphologically distinct forms co-occur .…”

“…The number of independent evolutionary lineages, partial lineages, or even lineages within lineages within Ensatina is a thorny empirical issue and open to debate (Highton, 1998;Wake and Schneider, 1998;Wake, 2006;Pereira and Wake, 2009). Here is the key point: even if one concludes that multiple independent metapopulation-level evolutionary lineages (i.e., species) are present within the Ensatina complex, the complex would remain a ring species because it possesses the pertinent biogeographic history Moritz et al, 1992;Kuchta et al, 2009a) and patterns of reproductive isolation (Wake, 1997;Alexandrino et al, 2005;Pereira and Wake, 2009;Devitt et al, 2011). These attributes do not change whether Ensatina is composed of one independent metapopulation-level evolutionary lineage or 20 such lineages.…”