Bending for love: losses and gains of sexual dimorphisms are strictly correlated with changes in the mounting position of sepsid flies (Sepsidae: Diptera).

Background: Sexually dimorphic structures contribute the largest number of morphological differences between closely related insect species thus implying that these structures evolve fast and are involved in speciation. The current literature focuses on the selective forces that drive these changes, be it 'sexual conflict' or 'female choice'. However, there are only few studies examining the function of sexual dimorphisms and even fewer that investigate how functional changes influence dimorphisms. This is largely due to the paucity of taxa for which the morphology, behavior, and phylogenetic relationships for multiple species are known. Here we present such data for sepsid flies. Sepsids have starkly dimorphic forelegs whose function can be documented under laboratory conditions. We use data from 10 genes to reconstruct the phylogenetic relationships for 33 species and test whether mounting positions are correlated with the presence and absence of sexual dimorphisms in the forelegs.

Results: The phylogenetic tree fully resolves the relationship with 29 of the 31 nodes of the tree having a posterior probability of 1.0. Twenty-eight of the 31 sepsid species have sexually dimorphic forelegs. All 28 species with such forelegs have the same mounting technique whereby the male uses his modified forelegs to grasp the female wingbase. Mapping mounting behavior and foreleg morphology onto the tree reveals that the wing grasp evolved once and was reduced twice. All changes in the mounting behavior are strictly and statistically significantly correlated with the origin and losses of sexually dimorphic legs (concentrated changes test: P < 0.001); i.e., the two species that have independently lost the wing grasp have both also re-evolved monomorphic legs. The wing grasp in these species is replaced with a novel but very similar mounting technique not involving the forelegs: the males bend their abdomens forward and directly establish genital contact to the female. In addition, one of the secondarily monomorphic species, Sepsis secunda, has evolved a new sexual dimorphism, a 'bump' on the dorsal side of the 4th tergite, which is now touching the ventral side of the female abdomen.

Conclusion: Our study reveals that the evolution of sexually dimorphic legs in Sepsidae can only be understood once the function of the legs during mating is considered and the relationships of species with and without sexual dimorphisms are known. We demonstrate that homoplasy in sexually dimorphic structures can be due to homoplasy in mating behavior. We furthermore document that the two species with secondarily monomorphic legs have independently replaced the typical sepsid wing grasp with very similar, new mounting techniques. This suggests that convergent evolution may be common in mating behaviors.