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

Coexisting plant congeners often experience strong competition for resources. Competition for pollinators can result in direct fitness costs via reduced seed set or indirect costs via heterospecific pollen transfer (HPT), causing subsequent gamete loss and unfit hybrid offspring production. Autonomous selfing may alleviate these costs, but to preempt HPT, selfing should occur early, before opportunities for HPT occur (i.e., "preemptive selfing hypothesis"). We evaluated conditions for this hypothesis in Collinsia sister species, C. linearis and C. rattanii. In field studies, we found virtually identical flowering times and pollinator sharing between congeners in sympatric populations. Compared to allopatric populations, sympatric C. linearis populations enjoyed higher pollinator visitation rates, whereas visitation to C. rattanii did not differ in sympatry. Importantly, the risk of HPT to each species in sympatry was strongly asymmetrical; interspecies visits comprised 40% of all flower-to-flower visits involving C. rattanii compared to just 4% involving C. linearis. Additionally, our greenhouse experiment demonstrated a strong cost of hybridization when C. rattanii was the pollen donor. Together, these results suggest that C. rattanii pays the greatest cost of pollinator sharing. Matching predictions of the preemptive selfing hypothesis, C. rattanii exhibit significantly earlier selfing in sympatric relative to allopatric populations.

Transcriptomic analysis links gene expression to unilateral pollen-pistil reproductive barriers.

BACKGROUND: Unilateral incompatibility (UI) is an asymmetric reproductive barrier that unidirectionally prevents gene flow between species and/or populations. UI is characterized by a compatible interaction between partners in one direction, but in the reciprocal cross fertilization fails, generally due to pollen tube rejection by the pistil. Although UI has long been observed in crosses between different species, the underlying molecular mechanisms are only beginning to be characterized. The wild tomato relative Solanum habrochaites provides a unique study system to investigate the molecular basis of this reproductive barrier, as populations within the species exhibit both interspecific and interpopulation UI. Here we utilized a transcriptomic approach to identify genes in both pollen and pistil tissues that may be key players in UI. RESULTS: We confirmed UI at the pollen-pistil level between a self-incompatible population and a self-compatible population of S. habrochaites. A comparison of gene expression between pollinated styles exhibiting the incompatibility response and unpollinated controls revealed only a small number of differentially expressed transcripts. Many more differences in transcript profiles were identified between UI-competent versus UI-compromised reproductive tissues. A number of intriguing candidate genes were highly differentially expressed, including a putative pollen arabinogalactan protein, a stylar Kunitz family protease inhibitor, and a stylar peptide hormone Rapid ALkalinization Factor. Our data also provide transcriptomic evidence that fundamental processes including reactive oxygen species (ROS) signaling are likely key in UI pollen-pistil interactions between both populations and species. CONCLUSIONS: Gene expression analysis of reproductive tissues allowed us to better understand the molecular basis of interpopulation incompatibility at the level of pollen-pistil interactions. Our transcriptomic analysis highlighted specific genes, including those in ROS signaling pathways that warrant further study in investigations of UI. To our knowledge, this is the first report to identify candidate genes involved in unilateral barriers between populations within a species.

Self-compatibility is over-represented on islands.

Because establishing a new population often depends critically on finding mates, individuals capable of uniparental reproduction may have a colonization advantage. Accordingly, there should be an over-representation of colonizing species in which individuals can reproduce without a mate, particularly in isolated locales such as oceanic islands. Despite the intuitive appeal of this colonization filter hypothesis (known as Baker's law), more than six decades of analyses have yielded mixed findings. We assembled a dataset of island and mainland plant breeding systems, focusing on the presence or absence of self-incompatibility. Because this trait enforces outcrossing and is unlikely to re-evolve on short timescales if it is lost, breeding system is especially likely to reflect the colonization filter. We found significantly more self-compatible species on islands than mainlands across a sample of > 1500 species from three widely distributed flowering plant families (Asteraceae, Brassicaceae and Solanaceae). Overall, 66% of island species were self-compatible, compared with 41% of mainland species. Our results demonstrate that the presence or absence of self-incompatibility has strong explanatory power for plant geographical patterns. Island floras around the world thus reflect the role of a key reproductive trait in filtering potential colonizing species in these three plant families.

Mating system transitions in Solanum habrochaites impact interactions between populations and species.

In 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 pollen-pistil 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 loss-of-function mutations, impact reproductive barriers within and between species.

The scope of Baker's law.

Baker's law refers to the tendency for species that establish on islands by long-distance dispersal to show an increased capacity for self-fertilization because of the advantage of self-compatibility when colonizing new habitat. Despite its intuitive appeal and broad empirical support, it has received substantial criticism over the years since it was proclaimed in the 1950s, not least because it seemed to be contradicted by the high frequency of dioecy on islands. Recent theoretical work has again questioned the generality and scope of Baker's law. Here, we attempt to discern where the idea is useful to apply and where it is not. We conclude that several of the perceived problems with Baker's law fall away when a narrower perspective is adopted on how it should be circumscribed. We emphasize that Baker's law should be read in terms of an enrichment of a capacity for uniparental reproduction in colonizing situations, rather than of high selfing rates. We suggest that Baker's law might be tested in four different contexts, which set the breadth of its scope: the colonization of oceanic islands, metapopulation dynamics with recurrent colonization, range expansions with recurrent colonization, and colonization through species invasions.

Comparative population genomics in Collinsia sister species reveals evidence for reduced effective population size, relaxed selection, and evolution of biased gene conversion with an ongoing mating system shift.

Selfing species experience reduced effective recombination rates and effective population size, which can lead to reductions in polymorphism and the efficacy of natural selection. Here, we use illumina transcriptome sequencing and population resequencing to test for changes in polymorphism, base composition, and selection in the selfing angiosperm Collinsia rattanii (Plantaginaceae) compared with its more outcrossing sister species Collinsia linearis. Coalescent analysis indicates intermediate species divergence (500,000-1 million years) with no ongoing gene flow, but also evidence that the C. rattanii clade remains polymorphic for floral morphology and mating system, suggesting either an ongoing shift to selfing or a potential reversal from selfing to outcrossing. We identify a significant reduction in polymorphism in C. rattanii, particularly within populations. Analysis of polymorphisms suggests an elevated ratio of unique nonsynonymous to synonymous polymorphism in C. rattanii, consistent with relaxed selection in selfing lineages. We additionally find higher linkage disequilibrium and differentiation, lower GC content at variable sites, and reduced expression of genes important in pollen production and pollinator attraction in C. rattanii compared with C. linearis. Together, our results highlight the potential for rapid shifts in the efficacy of selection, gene expression and base composition associated with ongoing evolution of selfing.

Developmental onset of reproductive barriers and associated proteome changes in stigma/styles of Solanum pennellii.

Although self-incompatibility (SI) in plants has been studied extensively, far less is known about interspecific reproductive barriers. One interspecific barrier, known as unilateral incongruity or incompatibility (UI), occurs when species display unidirectional compatibility in interspecific crosses. In the wild tomato species Solanum pennellii, both SI and self-compatible (SC) populations express UI when crossed with domesticated tomato, offering a useful model system to dissect the molecular mechanisms involved in reproductive barriers. In this study, the timing of reproductive barrier establishment during pistil development was determined in SI and SC accessions of S. pennellii using a semi-in vivo system to track pollen-tube growth in developing styles. Both SI and UI barriers were absent in styles 5 days prior to flower opening, but were established by 2 days before flower opening, with partial barriers detected during a transition period 3-4 days before flower opening. The developmental expression dynamics of known SI factors, S-RNases and HT proteins, was also examined. The accumulation of HT-A protein coincided temporally and spatially with UI barriers in developing pistils. Proteomic analysis of stigma/styles from key developmental stages showed a switch in protein profiles from cell-division-associated proteins in immature stigma/styles to a set of proteins in mature stigma/styles that included S-RNases, HT-A protein and proteins associated with cell-wall loosening and defense responses, which could be involved in pollen-pistil interactions. Other prominent proteins in mature stigma/styles were those involved in lipid metabolism, consistent with the accumulation of lipid-rich material during pistil maturation.

Can differences in autonomous selfing ability explain differences in range size among sister-taxa pairs of Collinsia (Plantaginaceae)? An extension of Baker's Law.

Species with greater selfing ability are predicted to be better adapted for colonizing new habitats (Baker's Law). Here, we tested an expansion of this hypothesis: that species proficient at autonomous selfing have larger range sizes than their less proficient sister taxa. We also tested competing hypotheses regarding seed production and niche breadth on range size. Floral traits affecting the proficiency of autonomous selfing were measured and seed production was calculated for six sister-taxa pairs in the clade Collinsia. We tested for the hypothesized effects of these variables on elevational distribution and range size. We found that species most proficient at selfing had significantly larger range sizes than their sister-taxa that were less proficient at selfing. Species proficient at autonomous selfing occupied a higher mean elevation than their sister taxa, but they did not differ in their total elevational range. Species with greater seed production did not have larger range sizes. Our results extend Baker's Law, suggesting that species proficient at autonomous selfing are better adapted to establish new populations and thus can more readily expand their range. Autonomous selfing ability may play a vital role in explaining variance in range size among other species.

Comparative approaches to the evolution of reproductive isolation: a comment on Scopece et al. 2007.

Speciation can be driven by the evolution of many forms of reproductive isolation. Comparative study is a powerful approach for elucidating the relative importance of individual isolating barriers in the speciation process. A recent contribution by Scopece and colleagues provides comparative data for two groups of deceptive pollination orchids and aims to test hypotheses about which forms of isolation are most important in the two clades. The authors compare pollinator isolation and postmating isolation between the two orchid groups, and conclude that food-deceptive orchid species have less isolation by pollinator specificity than sexually deceptive species, and that postmating isolation is more important in the food-deceptive clade. Although we find this approach to be novel and potentially powerful, these conclusions are called into question by the methods used to define and select species and quantify pollinator isolation. Definition and selection of taxa were performed in a biased manner that undermines the ability to infer general patterns of speciation. Furthermore, pollinator isolation was calculated inconsistently for the two groups under study, effectively nullifying the comparison.