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

Abstract

Hybridization 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.

Population genomics indicates micro‐refuges and riverine barriers for a southern South American grassland nightshade

“…The sampling also aligns with other studies conducted with Petunia species (e.g. Caballero‐Villalobos et al, 2021; our group unpublished data) based on single nucleotide polymorphisms. All geographical coordinates of collection sites were obtained using a Global Positioning System (GPS) unit per collection site (Table S1).…”

Could the reproductive system explain the stability and long-term persistence in a natural hybrid zone of Petunia (Solanaceae)?

“…In nature, just a few hybrid morphotypes were found outside shelters together with canonical P. axillaris individuals (Turchetto et al 2019a;b;Schnitzler et al 2020;Teixeira et al 2020), which reinforces the idea of a well-established system protecting P. axillaris from gene exchanging with a sympatric congener. Moreover, the same gene set that allowed P. exserta divergence and adaptation to a particular environment could restrict hybrids' development outside the shelters (Caballero-Villalobos et al 2021).…”

“…However, species' integrity can also be maintained by postzygotic isolating that limits the fitness of hybrids (Coyne & Orr 2004). The most limiting barrier for these Petunia species and their hybrids establishment seems to be the environmental differential selection (Caballero-Villalobos et al 2021) that could prevent the development of P. axillaris inside caves and almost totally prevent hybrids growth outside shelters.…”

Genetic architecture of a pollinator shift and its fate in secondary hybrid zones of two Petunia species

“…In the two known cases where P. axillaris and P. exserta are not isolated by geography, the species hybridise in secondary contact zones [ 44 ]. A recent study estimated this secondary contact of the species to be recent (approximately 920 years ago) and ongoing [ 45 ]. Although interspecific hybrids can produce viable offspring and can be found within the hybrid zones, individuals displaying the pure P. axillaris and P. exserta phenotypes are found at relatively high frequency [ 44 , 46 – 48 ].…”

“…Although interspecific hybrids can produce viable offspring and can be found within the hybrid zones, individuals displaying the pure P. axillaris and P. exserta phenotypes are found at relatively high frequency [ 44 , 46 – 48 ]. This suggests partial reproductive isolation between the species upon secondary contact, likely due to their different pollination syndromes [ 45 , 49 – 52 ].…”