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Although flowering traits are often assumed to be under strong selection by pollinators, significant variation in such traits remains the norm for most plant species. Thus, it is likely that the interactions among plants, mutualists, and other selective agents, such as antagonists, ultimately shape the evolution of floral and flowering traits. We examined the importance of pollination vs pre‐dispersal seed predation to selection on plant and floral characters via female plant‐reproductive success in Castilleja linariaefolia (Scrophulariaceae). C. linariaefolia is pollinated by hummingbirds and experiences high levels of pre‐dispersal seed predation by plume moth and fly larvae in the Rocky Mountains of Colorado, USA, where this work was conducted. We first examined whether female reproduction in C. linariaefolia was limited by pollination. Supplemental pollination only marginally increased components of female reproduction, likely because seed predation masked, in part, the beneficial effects of pollen addition. In unmanipulated populations, we measured calyx length, flower production, and plant height and used path analysis combined with structural equation modeling to quantify their importance to relative seed set through pathways involving pollination vs seed predation. We found that the strength of selection on calyx length, flower production, and plant height was greater for seed predation pathways than for pollination pathways, and one character, calyx length, experienced opposing selection via pollination vs seed predation. These results suggest that the remarkable intraspecific variation in plant and floral characters exhibited by some flowering plants is likely the result of selection driven, at least in part, by pollinators in concert with antagonists, such as pre‐dispersal seed predators. This work highlights the subtle but complex interactions that shape floral and vegetative design in natural ecosystems.
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