SUMMARYWild tomato species in Solanum Section Lycopersicon often exhibit two types of reproductive barriers: selfincompatibility (SI) and unilateral incompatibility or incongruity (UI), wherein the success of an inter-specific cross depends on the direction of the cross. UI pollen rejection often follows the 'SI · SC' rule, i.e. pistils of SI species reject the pollen of SC (self-compatible) species but not vice versa, suggesting that the SI and UI pollen rejection mechanisms may overlap. In order to address this question, pollen tube growth was measured after inter-specific crosses using wild tomato species as the female parents and pollen from cultivated tomato (Solanum lycopersicum). Two modes of UI pollen rejection, early and late, were observed, and both differed from SI pollen rejection. The structure and expression of known stylar SI genes were evaluated. We found that S-RNase expression is not required for either the early or late mode of UI pollen rejection. However, two HT family genes, HT-A and HT-B, map to a UI QTL. Surprisingly, we found that a gene previously implicated in SI, HT-B, is mutated in both SI and SC S. habrochaites accessions, and no HT-B protein could be detected. HT-A genes were detected and expressed in all species examined, and may therefore function in both SI and UI. We conclude that there are significant differences between SI and UI in the tomato clade, in that pollen tube growth differs between these two rejection systems, and some stylar SI factors, including S-RNase and HT-B, are not required for UI.
SummaryIn plants, transitions in mating system from outcrossing to self-fertilization are common; however, the impact of these transitions on interspecific and interpopulation reproductive barriers is not fully understood. We examined the consequences of mating system transition for reproductive barriers in 19 populations of the wild tomato species Solanum habrochaites.We identified S. habrochaites populations with self-incompatible (SI), self-compatible (SC) and mixed population (MP) mating systems, and characterized pollen-pistil interactions among S. habrochaites populations and between S. habrochaites and other tomato species. We examined the relationship between mating system, floral morphology, interspecific and interpopulation compatibility and pistil SI factors.We documented five distinct phenotypic groups by combining reproductive behavior with molecular data. Transitions from SI to MP were not associated with weakened interspecific reproductive barriers or loss of known pistil SI factors. However, transitions to SC at the northern range margin were accompanied by loss of S-RNase, smaller flowers, and weakened (or absent) interspecific pollenÀpistil barriers. Finally, we identified a subset of SC populations that exhibited a partial interpopulation reproductive barrier with central SI populations.Our results support the hypothesis that shifts in mating system, followed by additional lossof-function mutations, impact reproductive barriers within and between species.
Premise Adaptation to harsh edaphic substrates has repeatedly led to the evolution of edaphic specialists and generalists. Yet, it is unclear what factors promote specialization versus generalization. Here, we search for habitat use patterns associated with serpentine endemics (specialists) and serpentine tolerators (generalists) to indirectly test the hypothesis that trade‐offs associated with serpentine adaptation promote specialization. We predict that (1) endemics have adapted to chemically harsher and more bare serpentine habitats than tolerators, and (2) edaphic endemics show more habitat divergence from their sister species than tolerators do among on‐ and off‐serpentine populations. Methods We selected 8 serpentine endemic and 9 serpentine tolerator species representing independent adaptation to serpentine. We characterized soil chemistry and microhabitat bareness from one serpentine taxon of each species and from a paired nonserpentine sister taxon, resulting in 8 endemic and 9 tolerator sister‐taxa pairs. Results We find endemic serpentine taxa occur in serpentine habitats averaging twice as much bare ground as tolerator serpentine taxa and 25% less soil calcium, a limiting macronutrient in serpentine soils. We do not find strong evidence that habitat divergence between sister taxa of endemic pairs is greater than between sister taxa of tolerator pairs. Conclusions These results suggest serpentine endemism is associated with adaptation to chemically harsher and more bare serpentine habitats. It may be that this adaptation trades off with competitive ability, which would support the longstanding, but rarely tested, competitive trade‐off hypothesis.
Understanding the relative importance of reproductive isolating mechanisms across the speciation continuum remains an outstanding challenge in evolutionary biology. Here, we examine a common isolating mechanism, reproductive phenology, between plant sister taxa at different stages of adaptive divergence to gain insight into its relative importance during speciation. We study 17 plant taxa that have independently adapted to inhospitable serpentine soils, and contrast each with a nonserpentine sister taxon to form pairs at either ecotypic or species-level divergence. We use greenhouse-based reciprocal transplants in field soils to quantify how often flowering time (FT) shifts accompany serpentine adaptation, when FT shifts evolve during speciation, and the genetic versus plastic basis of these shifts. We find that genetically based shifts in FT in serpentine-adapted taxa are pervasive regardless of the stage of divergence. Although plasticity increases FT shifts in five of the pairs, the degree of plasticity does not differ when comparing ecotypic versus species-level divergence. FT shifts generally led to significant, but incomplete, reproductive isolation that did not vary in strength by stage of divergence. Our work shows that adaptation to a novel habitat may predictably drive phenological isolation early in the speciation process.
Theory predicts that the ability for natural selection to remove deleterious mutations from a population, and prevent the accumulation of genetic load, is a function of the effective population size (Ne). Shifts from random mating to self-fertilization (selfing) are predicted to decrease Ne through a variety of genomic changes - including a reduction in effective recombination and an increase in homozygosity. While a long history of theory suggests that the efficacy of selection, particularly against non-recessive mutations, should decrease with selfing rate, comparisons of genomic-based estimates of the efficacy of selection between related outcrosser-selfer pairs have revealed conflicting results. We address this paradox by simulating the evolution of strongly deleterious recessive and weakly deleterious additive mutations across a range of recombination, mutation and selective parameter combinations. We find that the genetic load of a population can either increase, decrease, or not vary with selfing rate. Genetic load is higher in selfers only when recombination rates are greater than mutation rates. When recombination rates are lower than mutation rates, an accumulation of recessive mutations leads to pseudo-overdominance, a type of balancing selection, in outcrossing populations. Using both simulations and analytical theory, we show that pseudo-overdominance has strong negative effects on the efficacy of selection against linked additive mutations and that a threshold level of selfing prevents pseudo-overdominance. Our results show that selection can be more or less effective in selfers as compared to outcrossers depending on the relationship between the deleterious mutation rate and gene density, and therefore different genomic regions in different taxa could show differing results.
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