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

Abstract

BackgroundSexually 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.ResultsThe 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.ConclusionOur 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.

The Role of Sexual Selection and Conflict in Mediating Among-Population Variation in Mating Strategies and Sexually Dimorphic Traits in Sepsis punctum

“…Both European and North American S. punctum males possess modified forelimbs including spines at the ventral margins of the forefemur, but the degree of forelimb elaboration is notably reduced in North America (Figure 1). Forelimb spines occur in 28 of the 31 sepsid species studied by Puniamoorthy et al [28], and their modification matches precisely the use of forelimbs for grasping females at the wing base during copulation. Such morphological modifications have been shown to confer an advantage in pre-copulatory struggles with unwilling females in several insect species, independent of body size [29]–[31], including in the closely related species Sepsis cynipsea , for which costs of mating and resistance have been demonstrated [32].…”

“…It therefore seems more probable that larger males achieve higher mating success as the result of either active or passive female preferences [16], [34]. In addition to the apparent advantage of a large male size, comparative evidence across the Sepsidae clearly demonstrates that male forelimb spines function in grasping the female wingbase [28], [48]. Whether their evolution is attributable to selection for male persistence in mating indicating sexual conflict is debated, however [16], [48].…”

Hidden in the urban parks of New York City: Themira lohmanus, a new species of Sepsidae described based on morphology, DNA sequences, mating behavior, and reproductive isolation (Sepsidae, Diptera)

“…Our description is part of a larger series of papers describing and investigating the mating behavior of sepsids (e.g. Ang et al 2008, 2013; Puniamoorthy et al 2008, 2009; Tan et al 2011, 2010). However, this is the first case in which a species that lacks species-specific behavioral elements.…”

Five additions to the list of Sepsidae (Diptera) for Vietnam: Perochaeta cuirassa sp. n., Perochaeta lobo sp. n., Sepsis spura sp. n., Sepsis sepsi Ozerov, 2003 and Sepsis monostigma Thompson, 1869

“…However, Perochaeta has secondarily reduced foreleg armature, and at least P. dikowi has evolved a novel mounting behavior that does not involve the foreleg grasp (Ang et al 2008). Th is has made Perochaeta a model for testing the correlation between the evolution of behavior and morphology (see Puniamoorthy et al 2008Puniamoorthy et al , 2009). …”