The evolution of multi-component weapons in the superfamily of leaf-footed bugs

Abstract

Sexually selected weapons, such as the antlers of deer, claws of crabs, and tusks of beaked whales, are strikingly diverse across taxa and even within groups of closely related species. Phylogenetic comparative studies have typically taken a simplified approach to investigating the evolution of weapon diversity, examining the gains and losses of entire weapons, major shifts in size or type, or changes in location. Less understood is how individual weapon components evolve and assemble into a complete weapon. We addressed this question by examining weapon evolution in the diverse, multi-component hind-leg and body weapons of leaf-footed bugs, Superfamily Coreoidea (Hemiptera: Heteroptera). Male leaf-footed bugs use their weapons to fight for access to mating territories. We used a large multilocus dataset comprised of ultraconserved element loci for 248 species and inferred evolutionary transitions among component states using ancestral state estimation. We found that weapons added components over time with some evidence of a cyclical evolutionary pattern -- gains of components followed by losses and then gains again. Further, we found that certain trait combinations evolved repeatedly across the phylogeny. This work reveals the remarkable and dynamic evolution of weapon form in the leaf-footed bugs. It also highlights that multi-component weapons may be especially useful in providing insights into the evolutionary interplay of form and function. TEASER TEXTFor centuries, humans have been fascinated by the morphological weapons animals use to engage in battle. The diversity of sexually selected weapons is surprising, with considerable variation across even closely related groups of animals. Studies are needed that take a detailed view of the components that comprise weapons and the evolutionary assembly of these components into a complete structure. Here, we reconstruct the evolution of a multi-component weapon in a superfamily of insects. Male leaf-footed bugs use spiky, enlarged hind legs to wrestle over mating territories. We measured 15 putative weapon components across 248 species, using phylogenetic comparative analyses. We found that the number of weapon components generally increased over time, with many gains and losses of components along the way. We found that certain components were more likely to evolve with others, suggesting that specific trait combinations might be especially functional in battle. This work highlights that evolutionary studies of complex, multi-component weapons may be useful for reconstructing the evolutionary assembly of weapons and the interplay of form and function.