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Abstract Characterizing the mechanisms of reproductive isolation between lineages is key to determining how new species are formed and maintained. In flowering plants, interactions between the reproductive organs of the flower—the pollen and the pistil—serve as the last barrier to reproduction before fertilization. As such, these pollen–pistil interactions are both complex and important for determining a suitable mate. Here, we test whether differences in style length (a part of the pistil) generate a postmating prezygotic mechanical barrier between five species of perennial Phlox wildflowers with geographically overlapping distributions. We perform controlled pairwise reciprocal crosses between three species with long styles and two species with short styles to assess crossing success (seed set). We find that the heterospecific seed set is broadly reduced compared to conspecific cross success and reveal a striking asymmetry in heterospecific crosses between species with different style lengths. To determine the mechanism underlying this asymmetric reproductive isolating barrier, we assess pollen tube growth in vivo and in vitro. We demonstrate that pollen tubes of short-styled species do not grow long enough to reach the ovaries of long-styled species. We find that short-styled species also have smaller pollen and that both within- and between-species pollen diameter is highly correlated with pollen tube length. Our results support the hypothesis that the small pollen of short-styled species lacks resources to grow pollen tubes long enough to access the ovaries of the long-styled species, resulting in an asymmetrical, mechanical barrier to reproduction. Such reproductive isolating mechanisms, combined with additional pollen–pistil incompatibilities, may be particularly important for closely related species in geographic proximity that share pollinators. 

The radiation of angiosperms is marked by a phenomenal diversity of floral size, shape, color, scent, and reward.1,2,3,4 The multi-dimensional response to selection to optimize pollination has generated correlated suites of these floral traits across distantly related species, known as “pollination syndromes.”5,6,7,8,9 The ability to test the broad utility of pollination syndromes and expand upon the generalities of these syndromes is constrained by limited trait data, creating a need for new approaches that can integrate vast, unstructured records from community-science platforms. Here, we compile the largest North American flower color dataset to date, using GPT-4 with Vision to classify color in over 11,000 species across more than 1.6 million iNaturalist observations. We discover that red- and orange-flowering species (classic “hummingbird pollination” colors) bloom later in eastern North America compared with other colors, corresponding to the arrival of migratory hummingbirds. Our findings reveal how seasonal flowering phenology, in addition to floral color and morphology, can contribute to the hummingbird pollination syndrome in regions where these pollinators are migratory. Our results highlight phenology as an underappreciated dimension of pollination syndromes and underscore the utility of integrating artificial intelligence with community-science data. The potential breadth of analysis offered by community-science datasets, combined with emerging data extraction techniques, could accelerate discoveries about the evolutionary and ecological drivers of biological diversity. 

• Reinforcement is the process through which prezygotic reproductive barriers evolve in sympatry due to selection against hybridization between co-occurring, closely related species. The role of self-fertilization in reinforcement and reproductive isolation is uncertain in part because its efficiency as a barrier against heterospecific mating can depend on the timing of autonomous selfing. • To investigate whether increased autonomous selfing has evolved as a mechanism for reinforcement, we compared Phlox cuspidata populations across their native Texas range using both estimates of genetic diversity and experimental manipulation with morphological measurements. Specifically, we investigated patterns of variation in floral traits and timing of selfing between individuals from allopatric populations of P. cuspidata and from populations sympatric with the closely related species, P. drummondii. • We infer intermediate rates of selfing across field-collected individuals with no significant difference between allopatric and sympatric populations. Among greenhouse grown plants, we find no differences in timing of selfing or other floral traits including anther dehiscence timing, anther-stigma distances, autonomous selfing rate and self-seed count between allopatric and sympatric populations. However, our statistical analyses indicate that P. cuspidata individuals sympatric with P drummondii seem to have generally larger flowers compared to allopatric individuals. • Despite strong evidence of costly hybridization with P. drummondii, we find no evidence of trait divergence due to reinforcement in P. cuspidata. Although we document nearly complete autonomous self-seed set in the greenhouse, estimates of selfing rates from genetic data imply realized selfing is much lower in nature suggesting an opportunity for reinforcing selection to act on this trait.