Museomics and protein-encoding ultraconserved elements illuminate the evolution of life history and phallic morphology of flesh flies (Diptera: Sarcophagidae)

Abstract

Background: The common name of the Flesh flies (Sarcophagidae) usually relates them with organisms feeding on decomposing organic matter, although the biology of one of the largest radiations among insects also includes predation, coprophagy, and even kleptoparasitism. The question of whether the ancestor of all sarcophagids was a predator or a decomposer, or in association to which host have sarcophagids evolved, has thus always piqued the curiosity of flesh fly specialists. Such curiosity has often been hindered by both the impossibility of having a well-supported phylogeny of Sarcophagidae and its sister group to trace live habits and the scarcity of information on the biology of the group. Using a phylogenomic dataset of ultraconserved elements from nearly all lineages of Sarcophagidae, a robust phylogenetic framework and timescale are generated to understand flesh fly systematics and the evolution of their life histories. Results: The evolutionary history for Sarcophagidae reconstructed here differs considerably from previous hypotheses. Within subfamily Sarcophaginae, a group of predatory flies, including genera Lepidodexia and Boettcheria, emerged as sister-group to the rest of Sarcophaginae. The genera Oxysarcodexia, Ravinia, and Tricharaea, long considered archaic and early-branching coprophagous and sarcosaprophagous lineages, were found nested well within the Sarcophaginae as sister-group to the sarcosaprophagous Microcerella. Predation on invertebrates is suggested as the ancestral and dominant strategy throughout the early evolution of flesh flies. Several switches from predation to sarcosaprophagy occur across the sarcophagid phylogenetic tree, in contrast with almost no switches from sarcosaprophagy or coprophagy to predatory habits. Regarding the morphological evolution of flesh flies, there might a concerted evolution of male genitalia traits, such as the phallotrema position and the juxta, or the vesica and the folding of the phallotrema. One diversification rate shift was inferred in the evolution of sarcophagids, which is associated with the genus Sarcophaga. Conclusions: This study has a significant impact on understanding sarcophagid evolution and highlights the importance of having a robust phylogenetic framework. I discuss the evolution of life histories of the family in relation to their hosts or substrates and outline how sarcosaprophagy, coprophagy, and kleptoparasitism behavior on various hosts may have evolved from predation on invertebrates. This study has established the framework for further physiological and comparative genomic work between predatory, sarcosaprophagous, coprophagous, and kleptoparasitic lineages, which could also have significant implications for the evolution of diverse life histories in other Diptera.