Divergence in style length and pollen size leads to a postmating‐prezygotic reproductive barrier among populations of Silene latifolia

Abstract

A central tenet of speciation research is the need to identify reproductive isolating barriers. One approach to this line of research is to identify the phenotypes that lead to reproductive isolation. Several studies on flowering plants have shown that differences in style length contribute to reproductive isolation between species, leading us to consider whether style length could act as a reproductive barrier among populations of a single species. This could occur if style length varied sufficiently and pollen size covaried with style length. Populations of Silene latifolia exhibit variation in flower size, including style length, that is negatively correlated with annual precipitation. We show that this divergence in style length has a genetic basis and acts as a reproductive barrier: males from small-flowered populations produced relatively small pollen grains that were poor at fertilizing ovules when crossed to females from large-flowered populations, leading to a significant reduction in seed production. Manipulating the distance pollen tubes had to travel revealed that this failure was purely mechanical and not the result of other incompatibilities. These results show that style length acts as a postmating-prezygotic reproductive barrier and indicate a potential link between ecotypic differentiation and reproductive isolation within a species.

Shifts to earlier selfing in sympatry may reduce costs of pollinator sharing

“…This pattern could reflect selection on the mating system in C. linearis through its ability to provide reproductive assurance rather than to serve as a barrier to HPT, driven by increased costs of earlier selfing via seed and ovule discounting in populations where visitation rates are high. While other studies have shown how general shifts to selfing were likely selected through the ability of selfing to reduce hybridization rates between outcrossing sister taxa (Fishman and Wyatt ; Smith and Rausher , ,b; Martin and Willis ; Brys et al., ; Briscoe‐Runquist and Moller ) or among lineages or populations within species (Goodwillie and Ness ; Martin et al ; Brothers and Delph ), only two others have also addressed the significance of the timing of selfing in reducing hybridization and thus reinforcing species’ boundaries. Both of these also found support for the preemptive selfing hypothesis.…”

Assessing biological factors affecting postspeciation introgression

“…In the first instance, mating system differences can cause predictable asymmetries in the success of initial crosses among species. This can occur either via differences in the size or shape of reproductive organs that can lead to asymmetric mechanical isolation among lineages (e.g., where outcrossing species can fertilize inbreeding species, but not vice versa; Levin ; Brothers and Delph ) or—especially in plants—via differences in the presence/absence of genetically determined self‐incompatibility systems, whereby pollen from self‐incompatible species can fertilize ovules of self‐compatible species, but self‐incompatible plants actively reject pollen from self‐compatible species (e.g., in Nicotiana : Anderson and de Winton ; Petunia : Mather and Edwardes ; and Solanum : McGuire and Rick ). In both mechanical and active‐rejection cases, outcrossing species are more likely to donate alleles to more inbreeding species compared to the reciprocal direction of gene flow, reducing the potential for gene flow specifically between species with unalike mating systems.…”

Insights into the genetic architecture of sexual dimorphism from an interspecific cross between two diverging Silene (Caryophyllaceae) species

“…We did not explore the first two options, but the F2 generation had a germination success of ≈80%, suggesting that failure at an early developmental stage could contribute to the observed segregation distortion. Also, earlier studies have shown that fertilization success can be affected by pollen competition between species (Rahmé, Widmer, & Karrenberg, ) and populations (Brothers & Delph, ).…”

“…It has been suggested that sexually selected traits evolve faster than other ecological traits (Mendelson, 2003) and contribute to the speciation process (Maan & Seehausen, 2011;Panhuis, Butlin, Zuk, & Tregenza, 2001;Servedio & Boughman, 2017). Previous studies in dioecious Silene evaluating differential scent production between males and females and the role of pollen competition in reproductive isolation suggested that sexual selection may be an important evolutionary driver in this species pair (Brothers & Delph, 2017;Rahmé et al, 2009;Waelti et al, 2009). In addition, there is evidence that ecological speciation is occurring between S. latifolia and S. dioica (Favre et al, 2016;Karrenberg & Favre, 2008).…”