Neutral and adaptive genomic variation in hybrid zones of two ecologically divergedPetuniaspecies (Solanaceae)

Abstract

AbstractHybridization between closely related plant species is a widespread phenomenon with significant evolutionary consequences, so natural hybrid zones provide exciting opportunities to study the processes of genetic differentiation and species formation. In Petunia, genetics, ecology and evolution of pollination syndromes have been thoroughly studied and related to the development of prezygotic isolation barriers between species. However, to date, no studies have explored the importance of extrinsic post-zygotic barriers such as environmental selection as drivers of reproductive isolation. In this study, we applied a population genetics approach to understand the speciation of two partially sympatric taxa of Petunia Juss that hybridize in the wild despite having strong differences in pollination syndrome, mating system and environmental requirements. We evaluated 58 individuals from seven allopatric and two contact zones of Petunia axillaris and P. exserta with genomic data to study the population genetic structure and gene exchange between these species and scan for potential loci under natural selection related to the preservation of species barriers. We explicitly evaluated the time, intensity and direction of interspecific migration, testing for alternative demographic scenarios. The genetic structure showed well-differentiated species-level lineages, and poor differentiation among populations of P. axillaris; P. exserta populations were highly structured, with several well-differentiated intraspecific lineages. Our data provide evidence for admixture with low asymmetric gene flow from P. axillaris to P. exserta associated with recent secondary contact, suggesting that pollinator specificity is not the only trait responsible for species integrity in this system. Combining the results from FST outlier and genotype–phenotype association methods, we identified 54 non-synonymous candidate variants under natural selection. Those variants are found in 35 coding sequences from which we found genes related to light-response networks, supporting that extrinsic factors such as habitat preferences can also provide a mechanism of reproductive isolation between Petunia spp. We argue that a set of pre- and post-zygotic barriers in conjunction with demographic processes maintain the species integrity.