POLLINATING SEED EATERS: WHY IS ACTIVE POLLINATION SO RARE?

Abstract

Insects whose larvae depend on developing seed are very common, but active pollination, meaning that the insect possesses specific structures and behaviors for the purpose of assuring pollination, is only known to have evolved twice in such insects, namely in yucca moths and in fig wasps. This rarity could be due to high cost of pollination, phylogenetic constraints, alternative life history shifts to reduce or avoid risk of seed nondevelopment, or ecological factors such as co-pollinators that can satiate pollen requirements and mask variation in pollinator effectiveness among ovipositing seed eaters. Ecological costs of being a pollinator were measured for a yucca moth species and were found to be low: active time allocated to pollen pickup and deposit was on average 4.1%, an average of 0.42% of female body mass was allocated to specific structures for pollen manipulation, and the average pollen load weighed <4% of moth body mass. These estimates suggest that ecological costs need not be a major obstacle to evolution of active pollination. In contrast, recent combined ecological–phylogenetic analyses for the yucca moth family suggest that the evolution of active pollination and transition to mutualism depended largely on preadaptations, and that few traits were truly novel. If general, active pollination would be predicted to be likely to evolve only in lineages with life histories that facilitate mutualism. Alternative outcomes to evolution of active pollination include delayed oviposition, detection of floral pollination status, egg placement that allows the larva to select a fruit, and modified egg dispersion strategies to balance the cost of pollination. The historical significance of these factors can be assessed only when mechanisms are documented in many lineages and analyzed in a phylogenetic framework. Active fungal inoculation among arthropods is ecologically analogous to active pollination, and offers a complement for comparative analyses. Specific structures for spore transport have evolved many times in at least three orders of insects, and several times in mites. The large number of independent lineages of active pollen and fungus dispersers jointly provide a platform for testing hypotheses about, e.g., the role of preadaptations in evolution of mutualism, reversals of mutualism, and the role of mutualism in diversification.