The cranial gland system of Nasonia spp.: a link between chemical ecology, evo-devo, and descriptive taxonomy (Hymenoptera: Chalcidoidea).

Abstract

Nasonia is an emerging model system for investigating the evolution of complex species-specific behavioral and morphological phenotypes. For example, the male head shape differs considerably between Nasonia Ashmead (Hymenoptera: Chalcidoidea) species. In addition, differences in courtship behaviors, and possibly influences of a male-specific aphrodisiac pheromone, contribute to interspecific prezygotic isolation. However, the possible relationships between courtship, pheromone signaling, and male head shape are unknown. Using multimodal imaging techniques, we conducted a comprehensive examination of the skeletomuscular and exocrine gland systems of the lower head region of all 4 Nasonia species and their sister genus Trichomalopsis Crawford (Hymenoptera: Chalcidoidea). This analysis reveals the presence of 3 undescribed exocrine glands in the lower head region and a unique mandibular modification, the basal mandibular carina, that might be involved in pheromone spread. We performed morphometric and volumetric analyses using 3D datasets from synchrotron X-ray microtomography and found that the size of the genomandibular gland and the corresponding basal mandibular carina correlates with both interspecific courtship length and head shape differences, indicating that this gland is a likely source of the oral aphrodisiac pheromone. These differences correlate with the prevalence of within-host mating rather than phylogenetic relatedness in Nasonia species, with increased within-host mating occurring in species with larger genomandibular glands. Our findings create an opportunity to better understand the complex gene regulatory networks underlying superficially unrelated traits and serve as a link between behavior, chemical ecology, evo-devo, and descriptive taxonomy.