skip to main content

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

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 investigate 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 morphological 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. Our results suggest that weapons added components over time with some evidence of a cyclical evolutionary pattern—gains of components followed by losses and then gains again. Furthermore, our best estimate indicated that certain trait combinations evolved repeatedly across the phylogeny, suggesting that they function together in battle or that they are genetically correlated. This work reveals the remarkable and dynamic evolution of weapon form in the leaf-footed bugs and provides insights into weapon assembly and disassembly over evolutionary time.

more » « less
Author(s) / Creator(s):
; ; ; ;
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    The evolution of sexually selected traits is a major topic in evolutionary biology. However, large-scale evolutionary patterns in these traits remain understudied, especially those traits used in male–male competition (weapons sensu lato). Here, we analyze weapon evolution in chamaeleonid lizards, both within and between the sexes. Chameleons are an outstanding model system because of their morphological diversity (including 11 weapon types among ~220 species) and a large-scale time-calibrated phylogeny. We analyze these 11 traits among 165 species using phylogenetic methods, addressing many questions for the first time in any group. We find that all 11 weapons have each evolved multiple times and that weapon origins are generally more frequent than their losses. We find that almost all weapons have each persisted for >30 million years (and some for >65 million years). Across chameleon phylogeny, we identify both hotspots for weapon evolution (up to 10 types present per species) and coldspots (all weapons absent, many through loss). These hotspots are significantly associated with larger male body size, but are only weakly related to sexual-size dimorphism. We also find that weapon evolution is strongly correlated between males and females. Overall, these results provide a baseline for understanding large-scale patterns of weapon evolution within clades.

    more » « less
  2. Abstract

    Theory predicts that traits with heightened condition dependence, such as sexually selected traits, should be affected by inbreeding to a greater degree than other traits. The presence of environmental stress may compound the negative consequences of inbreeding depression. In this study, we examined inbreeding depression across multiple traits and whether it increased with a known form of environmental stress. We conducted our experiment using both sexes of the sexually dimorphic leaf-footed cactus bug, Narnia femorata (Hemiptera: Coreidae). Adult male cactus bugs have enlarged hind legs used as weapons in male–male contests; these traits, and their homologue in females, have been previously found to exhibit high condition dependence. In this study, we employed a small developmental group size as an environmental stress challenge. Nymph N. femorata aggregate throughout their juvenile stages, and previous work has shown the negative effects of small group size on survivorship and body size. We found evidence of inbreeding depression for survival and seven of the eight morphological traits measured in both sexes. Inbreeding depression was higher for the size of the male weapon and the female homolog. Additionally, small developmental group size negatively affected survival to adulthood. However, small group size did not magnify the effects of inbreeding on morphological traits. These findings support the hypothesis that traits with heightened condition dependence exhibit higher levels of inbreeding depression.

    more » « less
  3. Abstract

    The size of weapons and testes can be central to male reproductive success. Yet, the expression of these traits is often extremely variable. Studies are needed that take a more complete organism perspective, investigating the sources of variation in both traits simultaneously and using developmental conditions that mimic those in nature. In this study, we investigated the components of variation in weapon and testis sizes using the leaf‐footed cactus bug,Narnia femorata(Hemiptera: Coreidae) on three natural developmental diets. We show that the developmental diet has profound effects on both weapon and testis expression and scaling. Intriguingly, males in the medium‐quality diet express large weapons but have relatively tiny testes, suggesting complex allocation decisions. We also find that heritability, evolvability, and additive genetic variation are highest in the high‐quality diet for testis and body mass. This result suggests that these traits may have an enhanced ability to respond to selection during a small window of time each year when this diet is available. Taken together, these results illustrate that normal, seasonal fluctuations in the nutritional environment may play a large role in the expression of sexually selected traits and the ability of these traits to respond to selection.

    more » « less
  4. Many sexually selected traits function as weapons, and these weapons can be incredibly diverse. However, the factors underlying weapon diversity among species remain poorly understood, and a fundamental hypothesis to explain this diversity remains untested. Although weapons can serve multiple functions, an undeniably important function is their role in fights. Thus, a crucial hypothesis is that weapon diversification is driven by the evolution of weapon modifications that provide an advantage in combat (e.g. causing more damage). Here, we test this fighting-advantage hypothesis using data from 17 species of coreid bugs. We utilize the fact that male–male combat in coreids often results in detectable damage, allowing us to link different weapon morphologies to different levels of damage among species. We find that certain weapon morphologies inflict much more damage than others, strongly supporting the fighting-advantage hypothesis. Moreover, very different weapon morphologies can inflict similarly severe amounts of damage, leading to a weapon performance landscape with multiple performance peaks. This multi-peak pattern could potentially drive different lineages towards divergent weapon forms, further increasing weapon diversity among species. Overall, our results may help explain how sexually selected weapons have evolved into the diversity of forms seen today. 
    more » « less
  5. Abstract

    A longstanding goal of evolutionary biology is to understand among-individual variation in resource allocation decisions and the timing of these decisions. Recent studies have shown that investment in elaborate and costly weapons can result in trade-offs with investment in testes. In this study, we ask the following questions: At what point plasticity in resource allocation to these different structures ceases during development, if at all? Furthermore, can individuals tailor their reproductive behavior to accompany structural changes? We experimentally addressed these questions in the insect Narnia femorata, quantifying resource reallocation across development for the first time, using a phenotypic engineering approach. To investigate whether allocation plasticity diminishes throughout ontogeny, we induced weapon loss at a range of different developmental stages and examined subsequent testes mass and reproductive behavior. We found that relative testes mass increased as weapon investment decreased, implying a direct trade-off between testes and weapon investment. However, autotomy postadulthood ceased to induce larger testes mass. Intriguingly, losing a weapon while young was associated with extended adult mating duration, potentially enabling compensation for reduced fighting ability. Our results highlight the importance of examining the ontogeny of trade-offs between reproductive traits and the flexibility of the relationship between reproductive morphology and behavior.

    more » « less