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Understanding how pollen moves between species is critical to understanding speciation, diversification, and evolution of flowering plants. For co-flowering species that share pollinators, competition through interspecific pollen transfer (IPT) can profoundly impact floral evolution, decreasing female fitness via heterospecific pollen deposition on stigmas and male fitness via pollen misplacement during visits to heterospecific flowers. The pollination literature demonstrates that such reproductive interference frequently selects for reproductive character displacement in floral traits linked to pollinator attraction, pollen placement, and mating systems and has also revealed that IPT between given pairs of species is typically asymmetric. More recent work is starting to elucidate its importance to the speciation process, clarifying the link between IPT and current and historical patterns of hybridization, the evolution of phenotypic novelty through adaptive introgression, and the rise of reproductive isolation. Our review aims to stimulate further research on IPT as a ubiquitous mechanism that plays a central role in angiosperm diversification.
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The effect of polyploidy and mating system on floral size and the pollination niche in Brassicaceae
Premise of research. Polyploidy, a major evolutionary process in flowering plants, is expected to 19 impact floral traits which can have cascading effects on pollination interactions, but this may 20 depend on selfing propensity. In a novel use of herbarium specimens, we assessed the effects of 21 polyploidy and mating system on floral traits and the pollination niche of 40 Brassicaceae 22 species. 23 Methodology. We combined data on mating system (self-compatible or self-incompatible) with 24 inferred ploidy level (polyploid or diploid) and use phylogenetically controlled analyses to 25 investigate their influence on floral traits (size and shape) and the degree of pollination 26 generalism based on the frequency and the richness of heterospecific pollen morphospecies 27 captured by stigmas. 28 Pivotal Results. Flower size (but not shape) depended on the interaction between ploidy and 29 mating system. Self-incompatible polyploid species had larger flowers than self-incompatible 30 diploids but there was no difference for self-compatible species. The breadth of pollination niche 31 (degree of generalism) was not affected by ploidy but rather strongly by mating system only. 32 Self-incompatible species had more stigmas with heterospecific pollen and higher heterospecific 33 pollen morphospecies richness per stigma than self-compatible species, regardless of their 34 ploidy. 35 Conclusions. Our results demonstrate that mating system moderated the influence of ploidy on 36 morphological features associated with pollination generalism but that response in terms of 37 heterospecific pollen captured as a proxy of pollination generalism was more variable.
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- Award ID(s):
- 2027604
- PAR ID:
- 10470850
- Publisher / Repository:
- University of Chicago Press
- Date Published:
- Journal Name:
- International Journal of Plant Sciences
- ISSN:
- 1058-5893
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract PremiseCo‐occurring plant species that share generalist pollinators often exchange pollen. This heterospecific pollen transfer (HPT) impacts male and female reproductive success through pollen loss and reductions in seed set, respectively. The resulting fitness cost of HPT imposes selection on reproductive traits (e.g., floral color and shape), yet we currently lack strong predictors for the post‐pollination fate of heterospecific pollen, especially within community and phylogenetic contexts. MethodsWe investigated the fate of heterospecific pollen at three distinct stages of plant reproduction: (1) pollen germination on the stigma, (2) pollen tube growth in the style, and (3) fertilization of ovules. We experimentally crossed 11 naturally co‐flowering species in the subalpine meadows of the Colorado Rocky Mountains, across a spectrum of phylogenetic relatedness. Using generalized linear mixed models and generalized linear models, we evaluated the effect of parental species identity and phylogenetic relatedness on pollen tube growth at each reproductive stage. ResultsWe found that heterospecific pollen tubes can germinate and grow within pistils at each reproductive stage, even when parental species are >100 My divergent. There was no significant effect of phylogenetic distance on heterospecific pollen success, and no evidence for a mechanism that suspends heterospecific pollen germination or pollen tube growth within heterospecific stigmas or styles. ConclusionsOur results show that even in communities where HPT is common, pre‐zygotic post‐pollination mechanisms do not provide strong barriers to interspecific fertilization. HPT can result in the loss of ovules even between highly diverged plant species.more » « less
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Summary If particular traits consistently affect rates of speciation and extinction, broad macroevolutionary patterns can be interpreted as consequences of selection at high levels of the biological hierarchy. Identifying traits associated with diversification rates is difficult because of the wide variety of characters under consideration and the statistical challenges of testing for associations from comparative phylogenetic data. Ploidy (diploid vs polyploid states) and breeding system (self‐incompatible vs self‐compatible states) are both thought to be drivers of differential diversification in angiosperms.We fit 29 diversification models to extensive trait and phylogenetic data in Solanaceae and investigate how speciation and extinction rate differences are associated with ploidy, breeding system, and the interaction between these traits.We show that diversification patterns in Solanaceae are better explained by breeding system and an additional unobserved factor, rather than by ploidy. We also find that the most common evolutionary pathway to polyploidy in Solanaceae occurs via direct breakdown of self‐incompatibility by whole genome duplication, rather than indirectly via breakdown followed by polyploidization.Comparing multiple stochastic diversification models that include complex trait interactions alongside hidden states enhances our understanding of the macroevolutionary patterns in plant phylogenies.more » « less
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Abstract Flowering plants have evolved numerous intraspecific and interspecific prezygotic reproductive barriers to prevent production of unfavourable offspring 1 . Within a species, self-incompatibility (SI) is a widely utilized mechanism that rejects self-pollen 2,3 to avoid inbreeding depression. Interspecific barriers restrain breeding between species and often follow the SI × self-compatible (SC) rule, that is, interspecific pollen is unilaterally incompatible (UI) on SI pistils but unilaterally compatible (UC) on SC pistils 1,4–6 . The molecular mechanisms underlying SI, UI, SC and UC and their interconnections in the Brassicaceae remain unclear. Here we demonstrate that the SI pollen determinant S -locus cysteine-rich protein/ S -locus protein 11 (SCR/SP11) 2,3 or a signal from UI pollen binds to the SI female determinant S -locus receptor kinase (SRK) 2,3 , recruits FERONIA (FER) 7–9 and activates FER-mediated reactive oxygen species production in SI stigmas 10,11 to reject incompatible pollen. For compatible responses, diverged pollen coat protein B-class 12–14 from SC and UC pollen differentially trigger nitric oxide, nitrosate FER to suppress reactive oxygen species in SC stigmas to facilitate pollen growth in an intraspecies-preferential manner, maintaining species integrity. Our results show that SRK and FER integrate mechanisms underlying intraspecific and interspecific barriers and offer paths to achieve distant breeding in Brassicaceae crops.more » « less
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1086/727826
