The evolution of intrinsic reproductive isolation in the genus Cakile (Brassicaceae)

Abstract

In theory, adaptive divergence can increase intrinsic post-zygotic reproductive isolation (RI), either directly via selection on loci associated with RI, or indirectly via linkage of incompatibility loci with loci under selection. To test this hypothesis, we measured RI at five intrinsic post-zygotic reproductive barriers between 18 taxa from the genera Cakile and Erucaria (Brassicaceae). Using a comparative framework, we tested whether the magnitude of RI was associated with genetic distance, geographic distance, ecological divergence and parental mating system. Early stages of post-zygotic RI related to F viability (i.e. initial seed set) tended to be stronger than later stages related to F fecundity (i.e. flower number, fruit number). Mating system significantly influenced early stages of RI, such that RI was lowest when the mother was selfing and father was outcrossing, consistent with an imbalance between sink strength and resistance to provisioning. We found little evidence that adaptive divergence accelerates the evolution of intrinsic post-zygotic RI, consistent with a nonecological model of evolution that predicts the nonlinear accumulation of RI and RI asymmetry with time (i.e. genetic distance), irrespective of adaptive divergence. Thus, although certain aspects of ecological divergence do not appear to have contributed strongly to the evolution of RI in this system, divergence in mating system actually reduced RI, suggesting that mating system evolution may play a significant role in speciation dynamics.

Along the speciation continuum: Quantifying intrinsic and extrinsic isolating barriers across five million years of evolutionary divergence in California jewelflowers

“…). Some systems however, exhibit no relationship between divergence time and intrinsic RI (e.g., Willis and Donohue ); this lack of association may be due to incompatibility mechanisms that evolve stochastically (Edmands ), or may result from a loss of power associated with phylogenetically corrected analyses (Jewell et al. ).…”

“…Our results contribute to a growing body of literature documenting the positive relationship between intrinsic RI and divergence time in plants (e.g., Glycine and Silene in Moyle et al 2004; Coreopsis in Archibald 2005; food-deceptive orchids in Scopece et al 2007;and Eucalyptus in Larcombe et al 2015). Some systems however, exhibit no relationship between divergence time and intrinsic RI (e.g., Willis and Donohue 2016); this lack of association may be due to incompatibility mechanisms that evolve stochastically (Edmands 2002), or may result from a loss of power associated with phylogenetically corrected analyses (Jewell et al 2012). Here we observe that F1 hybrids derived from recently diverged parents typically only suffer a small reduction in fitness compared to conspecific offspring, however hybrids from more diverged parents often show substantial decreases in fitness resulting from intrinsic incompatibilities (Figs.…”

Intraspecific variation in reproductive barriers between two closely related Arabidopsis sister species

“…An increase in postzygotic barriers has classically been attributed to the accumulation of genetic incompatibilities between diverging lineages (Orr, 1995). This pattern has been found particularly in allopatric species (Baack et al, 2015;Christie & Strauss, 2018;Coyne & Orr, 1997;Lowry et al, 2008;Matute & Cooper, 2021;Turissini et al, 2018;Willis & Donohue, 2017) and recently also between isolated lineages within a species (Barnard-Kubow & Galloway, 2017). Beyond, our results reject the hypothesis that prezygotic barriers are generally stronger than postzygotic barriers (Lowry et al, 2008), but they are in line with postzygotic barriers being more likely to evolve in allopatry (Ravinet et al, 2017) and prezygotic barriers when species once were in contact and shared gene flow (Butlin & Smadja, 2018).…”

“…This seems to apply particularly to genetically determined postzygotic barriers and species that evolve in allopatry (Ravinet et al, 2017 ), when closely related lineages become geographically isolated and diverge through genetic drift and selection, which result in the accumulation of RI (Orr, 1995 ). In contrast, increasing RI with increasing divergence time seems less consistent for prezygotic barriers (Christie & Strauss, 2018 ; Widmer et al, 2009 ; Willis & Donohue, 2017 ). Prezygotic barriers may evolve through different processes, such as reinforcement upon secondary contact, whereby selection leads to rapid accumulation of several such barriers (Butlin & Smadja, 2018 ).…”

“…A consequence of the diversity of processes and factors affecting the timing and strength of reproductive barriers is that RI may also vary depending on the population pairs used for interspecific contrasts. The patterns underlying variation in RI have been explored mostly between species without assessing intraspecific variation (Baack et al, 2015 ; Jewell et al, 2012 ; Lowry et al, 2008 ; Matute & Cooper, 2021 ; Moyle et al, 2004 ; Ramsey et al, 2003 ; Turissini et al, 2018 ; Widmer et al, 2009 ; Willis & Donohue, 2017 ). Only few studies compared the timing or strength of RI among replicate population pairs between two species, despite compelling evidence that RI may be heterogeneous depending on the populations under study (Christie & Strauss, 2019 ; Cutter, 2012 ; Zuellig & Sweigart, 2018 ).…”