Genomic discordance throws a wrench in the parallel speciation hypothesis for scincid lizards.

Abstract

Parallel evolution of the same reproductive isolation barrier within a taxon is an indicator of ecology's role in speciation (i.e., parallel speciation), yet spatiotemporal variability in the efficacy of the barrier can present challenges to retracing how it evolved. Here, we revisit the evidence for a candidate example of parallel speciation in a clade of scincid lizards (the Plestiodon skiltonianus complex) using genomic data, with emphasis on determining whether hybridization may have confounded the phylogenetic signals of parallelism for this group. Our results show a striking case of genealogical discordance, in which mitochondrial loci support multiple origins of a derived large-bodied morphotype (Plestiodon gilberti) within a small-bodied ancestor (Plestiodon skiltonianus), whereas nuclear loci indicate a single origin. We attribute the discordance to separate, temporally-spaced hybridization events that led to asymmetric capture of P. skiltonianus mitochondria in different regional lineages of P. gilberti. Nuclear introgression showed a similar directional bias but was less pervasive. We demonstrate how a mechanical reproductive barrier previously identified for this group explains the asymmetry of mitochondrial introgression, given that hybrid matings are most likely when the male is P. gilberti and the female is P. skiltonianus. We then use permutation tests of morphological data to provide evidence that the mechanical barrier is less stringent in areas where hybridization is inferred to have occurred. Our results demonstrate how biased hybridization can dictate which genetic variants are transmitted between species and emphasize the importance of accounting for introgression and deep coalescence in identifying phyletic signatures of parallel speciation.