The Evolution of Sexually Selected Traits - Comparative Morphology and Chemistry of the Cephalic Glands of Beewolves (Hymenoptera, Crabronidae)

The concept of evolution by natural selection, leading to the gradual adaptation of populations over time, has first been outlined by Charles Darwin. Generally, naturally selected traits evolve to maximize fitness in a given environment. Yet, already Darwin noted the existence of, often flamboyant, traits that are restricted to one sex and cannot possibly serve the fitness of their bearers under natural selection, like for example the enormous tail of a peacock. To explain the existence of such traits, Darwin invoked the concept of sexual selection, which maximizes the attractiveness (i.e. reproductive success) of their bearers, often at the expense of survival. Generally, sexual selection is assumed to lead to rapid evolutionary changes and promote population divergence and speciation. Yet, one major drawback in the study of sexual selection is that its actual impact on the variation of a trait cannot be separated from other evolutionary forces potentially contributing to observed trait variation, like natural selection, genetic drift, or mutation. The head glands of the digger wasp subfamily Philanthinae (Hymenoptera, Crabronidae) provide a suitable model system to study the evolution of interspecific variation in a trait under natural and sexual selection, respectively. Both the mandibular gland (MG) and the postpharyngeal gland (PPG) are present in both sexes of the Philanthinae, yet are under natural selection in females, but under sexual selection in males. Female Philanthinae provision their offspring with paralyzed insects, mostly other Hymenoptera and Coleoptera, that are stored in subterranean brood cells, where they are exposed to a high risk of fungal infestation. Female Philanthus triangulum and Trachypus elongatus are known to embalm their prey with high amounts of unsaturated hydrocarbons (HCs) from their large and complex PPGs. This so-called ‘prey embalming’ reduces the condensation of water on the prey’s cuticle und retards fungal growth. Based on chemical investigations of provisioned prey, the same mechanism is now proposed for Philanthus gibbosus, suggesting that this unique antimicrobial parental care behavior is common in all Philanthini. This hypothesis is further corroborated by the fact that all investigated females of this tribe possess uniform, complex PPGs, the secretions of which contain predominantly unsaturated HCs. Results are mixed, however, for the other two philanthine tribes, the Cercerini and Aphilanthopsini. While all investigated species of these tribes possessing small, simple PPGs, the chemical composition of their secretions varies, with some species being dominated by methyl-branched HCs, but some possessing considerable proportions of unsaturated HCs, thus resembling the Philanthini. Taken together, at least in the Philanthini, the PPG of females is under stabilizing natural selection due to its involvement in antimicrobial prey embalming. Males Philanthinae establish territories by scent marking with a sex pheromone, which is arguably the sole means to attract receptive females. In P. triangulum, the pheromone is produced and stored in the MG and PPG, and the same likely holds true for other male Philanthinae. Therefore, these glands should be under strong sexual selection. According to the theory that sexually selected traits should show high interspecific variation, there is tremendous diversity in gland morphology among male Philanthinae, regarding the occurrence of single gland reservoirs, their size and shape, as well as the type of associated secretory cells. There is, however, also an overall phylogenetic trend. Male Cercerini and Aphilanthopsini possess enormously large MGs, yet small and simple PPGs. In the Philanthini the size and complexity of the MG is reduced, while their PPG is considerably enlarged, more complex, and associated with complexes of secretory cells. In some clades of the Philanthini the MG is even lost and entirely replaced by the PPG. The amount of interspecific variation in head gland morphology is significantly higher among male than among female Philanthinae. According to preliminary results, there is likewise also marked interspecific variation in pheromone composition, with not one investigated species pair possessing the same combination of main pheromone constituents. In summary, the Philanthinae provide an ideal model for studying the evolution of shared traits under differential selection regimes. This model allows for the direct assessment of interspecific variation caused by different selection pressures, thereby corroborating the often proposed diversifying nature of sexual selection