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.
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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- Award ID(s):
- 2226881
- PAR ID:
- 10497033
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Evolution
- Volume:
- 78
- Issue:
- 4
- ISSN:
- 0014-3820
- Format(s):
- Medium: X Size: p. 635-651
- Size(s):
- p. 635-651
- Sponsoring Org:
- National Science Foundation
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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. -
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Abstract Allometry is the scaling relationship between a trait and body size. This relationship can often explain considerable morphological variation within and among species. Nevertheless, much remains unknown about the factors that underlie allometric patterns. For example, when different allometric relationships are observed amongst closely related species, these differences are regularly considered to be products of selection. However, directional selection on allometry (particularly the slope) has rarely been tested and observed in natural populations. Here, we investigate selection on the scaling relationship between weapon size and body size (i.e., weapon allometry) in a wild population of giant mesquite bugs, Pachylis neocalifornicus (previously Thasus neocalifornicus). Males in this species use their weapons (enlarged femurs) to compete with one another over access to resources and females. We found that large males with relatively large weapons successfully secured access to mates. However, we also found that small males with relatively small weapons could access mates as well. These two patterns together can increase the allometric slope of the sexually selected weapon, suggesting a straightforward process by which the allometric slope can evolve.
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Summary Global change has accelerated local species extinctions and colonizations, often resulting in losses and gains of evolutionary lineages with unique features. Do these losses and gains occur randomly across the phylogeny?
We quantified: temporal changes in plant phylogenetic diversity (PD); and the phylogenetic relatedness (PR) of lost and gained species in 2672 semi‐permanent vegetation plots in European temperate forest understories resurveyed over an average period of 40 yr.
Controlling for differences in species richness, PD increased slightly over time and across plots. Moreover, lost species within plots exhibited a higher degree of PR than gained species. This implies that gained species originated from a more diverse set of evolutionary lineages than lost species. Certain lineages also lost and gained more species than expected by chance, with Ericaceae, Fabaceae, and Orchidaceae experiencing losses and Amaranthaceae, Cyperaceae, and Rosaceae showing gains. Species losses and gains displayed no significant phylogenetic signal in response to changes in macroclimatic conditions and nitrogen deposition.
As anthropogenic global change intensifies, temperate forest understories experience losses and gains in specific phylogenetic branches and ecological strategies, while the overall mean PD remains relatively stable.
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From deer antlers to crab claws, weapons are some of the most elaborate and enormous structures in the animal kingdom. Within a species, weapon size generally increases with the size and condition of an individual, and those with larger weapons are usually better at fending off more diminutive competitors. Although it may seem desirable for all individuals to have large weapons, size varies greatly within a species. The ‘handicap principle’ proposes that the cost of bearing a weapon dictates the variation in weapon size. Smaller or less fit individuals pay more for weapons than larger or fitter animals, so smaller individuals tend to grow smaller weapons. Although popular, only a handful of studies have demonstrated experimental evidence that supports this theory. To test the handicap principle, Dinh and Patek studied a group of crustaceans known as snapping shrimp. Each shrimp has one enlarged claw that it uses as a weapon to fire imploding vapor bubbles at opponents during fights. Larger snapping shrimp have bigger enlarged claws and tend to win more contests. Males also have larger weapons than females, and this sex difference is amplified during the breeding season. Dinh and Patek studied weapon size in several species of snapping shrimp. Measurements showed that after controlling for body size, individuals with larger weapons had smaller abdomens, suggesting there is a tradeoff between weapon size and abdomen size. Furthermore, small males exhibited the steepest tradeoff, in line with the handicap principle. Snapping shrimp also showed sex-specific costs and benefits. After controlling for body size, females with larger weapons produced fewer and smaller eggs, while males with larger weapons were more likely to be paired with females and generally paired with larger females. This suggests that weapons are particularly burdensome to female shrimp and particularly beneficial to males, especially during the breeding season. These findings provide elusive evidence for the handicap principle and extend the theory to explain sex and seasonal differences in the size of snapping shrimp weapons. More broadly, the findings highlight the value of studying both male and female animal weapons when, historically, the focus has been on male weaponry.more » « less
