Active pollination drives selection for reduced pollen‐ovule ratios

Abstract

Premise Variation in pollen‐ovule ratios is thought to reflect the degree of pollen transfer efficiency—the more efficient the process, the fewer pollen grains needed. Few studies have directly examined the relationship between pollen‐ovule ratio and pollen transfer efficiency. For active pollination in the pollination brood mutualisms of yuccas and yucca moths, figs and fig wasps, senita and senita moths, and leafflowers and leafflower moths, pollinators purposefully collect pollen and place it directly on the stigmatic surface of conspecific flowers. The tight coupling of insect reproductive interests with pollination of the flowers in which larvae develop ensures that pollination is highly efficient. Methods We used the multiple evolutionary transitions between passive pollination and more efficient active pollination to test if increased pollen transfer efficiency leads to reduced pollen‐ovule ratios. We collected pollen and ovule data from a suite of plant species from each of the pollination brood mutualisms and used phylogenetically controlled tests and sister‐group comparisons to examine whether the shift to active pollination resulted in reduced pollen‐ovule ratios. Results Across all transitions between passive and active pollination in plants, actively pollinated plants had significantly lower pollen‐ovule ratios than closely related passively pollinated taxa. Phylogenetically corrected comparisons demonstrated that actively pollinated plant species had an average 76% reduction in the pollen‐ovule ratio. Conclusions The results for active pollination systems support the general utility of pollen‐ovule ratios as indicators of pollination efficiency and the central importance of pollen transfer efficiency in the evolution of pollen‐ovule ratio.

Sex allocation in dynamic mating environments

“…Loss from a mating arena is equivalent to propagule death, and one well known interspeci c pattern concerning pollen loss involves pollen:ovule ratios, which tend to decline among species whose oral visitors provide superior pollination service 76,77 . These patterns are commonly interpreted in terms of the e ciency of pollen transfer [76][77][78][79] , the proportion of pollen grains eventually deposited on stigmatic surfaces. But there is no theoretical basis for thinking that selection responds to e ciency per se 32 .…”

Bee-Mediated Selection Favors Floral Sex Specialization in a Heterantherous Species: Strategies to Solve the Pollen Dilemma

“…More interestingly, we detected that this variation translates into a significant vibrating bee-mediated selection towards flower's sexual specialization through both seed number and pollen removal, favouring male-biased individuals that release higher amounts of pollen grains and with intermediate heteranthery degrees, and S-or L-styled individuals with high female reproductive success within populations. The factors associated to the variation in the phenotypic gender, and the morphology of floral sexual organs, such as breeding system, successional stage, pollen transfer efficiency, and reproductive success in animal-pollinated plants have been broadly considered in the literature [39,40]. However, the effects of the selection exerted by pollinators on the set of these floral traits in natural populations have so far been neglected.…”

Interactions Between Figs and Gall-Inducing Fig Wasps: Adaptations, Constraints, and Unanswered Questions

“…Actively pollinated figs usually have smaller pollen-ovule ratios compared to those with passive pollination since there is much less pollen wastage and more precise pollen deposition (Pellmyr et al, 2020; but see Deng et al, 2016). Pollinator traits for active pollination (pro-thoracic pockets, coxal combs for pollen removal from the pockets) appear labile and track pollen-ovule ratios of associated fig species (Cook et al, 2004).…”