Lineages ofSilene nutansdeveloped rapid, strong, asymmetric postzygotic reproductive isolation in allopatry

Abstract

Reproductive isolation can rise either as a consequence of genomic divergence in allopatry or as a byproduct of divergent selection in parapatry. To determine whether reproductive isolation in gynodioecious Silene nutans results from allopatric divergence or from ecological adaptation following secondary contact, we investigated the pattern of postzygotic reproductive isolation and hybridization in natural populations using two phylogeographic lineages, western (W1) and eastern (E1). Experimental crosses between the lineages identified strong, asymmetric postzygotic isolation between the W1 and the E1 lineages, independent of geographic overlap. The proportion of ovules fertilized, seeds aborted, and seeds germinated revealed relatively little effect on the fitness of hybrids. In contrast, hybrid mortality was high and asymmetric: while half of the hybrid seedlings with western lineage mothers died, nearly all hybrid seedlings with E1 mothers died. This asymmetric mortality mirrored the proportion of chlorotic seedlings, and is congruent with cytonuclear incompatibility. We found no evidence of hybridization between the lineages in regions of co-occurrence using nuclear and plastid markers. Together, our results are consistent with the hypothesis that strong postzygotic reproductive isolation involving cytonuclear incompatibilities arose in allopatry. We argue that the dynamics of cytonuclear gynodioecy could facilitate the evolution of reproductive isolation.

Congruent population genetic structures and divergence histories in anther‐smut fungi and their host plants Silene italica and the Silene nutans species complex

“…We performed parameter inferences for the group of four models with ancient migration (“round 3, step 2,” group 3 see Table 1; Table ). The inferred dates and order of divergence between fungal genetic clusters parasitizing S. nutans were consistent with the history of divergence previously inferred for the host plant S. nutans (Figure 4; Martin et al, 2016, 2017; Van Rossum et al, 2018).…”

“…Within S. nutans , we identified four distinct haplotypes based on the six plastid SNPs, retrieving in our sample the four major genetic lineages of S. nutans previously identified in Western Europe (Figure 1a; Martin et al, 2016, 2017; Van Rossum et al, 2018). The blue, yellow, orange and red haplotypes were found, as in previous studies, in the northeastern, southeastern, western and southwestern parts of Europe, respectively.…”

“…We could not obtain enough fresh material for this study to be able to test local adaptation. Furthermore, strong asymmetric postzygotic reproductive isolation was found between the Eastern and Western S. nutans plant lineages (Martin et al, 2017), and it would be interesting in future studies to explore if a similar reproductive isolation pattern is present between the Eastern and Western fungal lineages on S. nutans , and whether reproductive isolation can be found among anther‐smut fungi.…”

“…To further genotype the plant individuals for studying the population genetic structure, we used a combination of plastid (chloroplast) SNPs and nuclear microsatellite markers as previously described (Godé et al, 2014; Martin et al, 2016, 2017). For plastid markers, using the KASPAR protocol we genotyped six SNPs, named Cp42, Cp397, Cp540, Cp656, Cp730 and Cp804, and polymorphic for [T/G], [A/C], [C/T], [G/T], [C/T] and [T/G], respectively.…”

A framework for estimating the effects of sequential reproductive barriers: Implementation using Bayesian models with field data from cryptic species

“…; Martin et al. ), we lack indices that can estimate directional (cross‐type‐specific) RI over an arbitrary combination of reproductive barriers, while controlling for contingency. Second, speciation research would benefit from more studies reporting and discussing uncertainty in RI (e.g., Merrill et al.…”