The typical pattern of morphological evolution associated with the radiation of a group of related species is the emergence of a novel trait and its subsequent diversification. Yet the genetic mechanisms associated with these two evolutionary steps are poorly characterized. Here, we show that a spot of dark pigment on fly wings emerged from the assembly of a novel gene regulatory module in which a set of pigmentation genes evolved to respond to a common transcriptional regulator determining their spatial distribution. The primitive wing spot pattern subsequently diversified through changes in the expression pattern of this regulator. These results suggest that the genetic changes underlying the emergence and diversification of wing pigmentation patterns are partitioned within genetic networks.

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.

All jumping spiders have unique, complex eyes with exceptional spatial acuity and some of the most elaborate vision‐guided predatory strategies ever documented for any animal of their size. However, it is only recently that phylogenetic techniques have been used to reconstruct the relationships and key evolutionary events within the Salticidae. Here, we used data for 35 species and six genes (4.8 kb) for reconstructing the phylogenetic relationships between Spartaeinae, Lyssomaninae and Salticoida. We document a remarkable case of morphological convergence of eye ultrastructure in two clades with divergent predatory behaviour. We, furthermore, find evidence for a stepwise, gradual evolution of a complex predatory strategy. Divergent predatory behaviour ranges from cursorial hunting to building prey‐catching webs and araneophagy with web invasion and aggressive mimicry. Web invasion and aggressive mimicry evolved once from an ancestral spartaeine that was already araneophagic and had no difficulty entering webs due to glue immunity. Web invasion and aggressive mimicry was lost once, in Paracyrba, which has replaced one highly specialized predation strategy with another (hunting mosquitoes). In contrast to the evolution of divergent behaviour, eyes with similarly high spatial acuity and ultrastructural design evolved convergently in the Salticoida and in Portia.