Large and exaggerated sexually selected weapons comprise high proportions of metabolically inexpensive exoskeleton

2023

eLife

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Evolutionary theory suggests that individuals should express costly traits at a magnitude that optimizes the cost-benefit difference for the trait-bearer. Trait expression varies across a species because costs and benefits vary among individuals. For example, if large individuals pay lower costs than small individuals, then larger individuals should reach optimal cost-benefit differences at a greater magnitude of trait expression. Using the remarkable cavitation-shooting weapons found in the big claws of male and female alpheid snapping shrimp, we test whether size- and sex-dependent expenditures explain the scaling of weapon size relative to body size and why males have larger proportional weapon size than females. We found that males and females from three snapping shrimp species (Alpheus heterochaelis, Alpheus angulosus, and Alpheus estuariensis) show patterns consistent with resource allocation tradeoffs between weapon and abdomen size. For male A. heterochaelis, the species for which we had the greatest sample size and statistical power, the smallest individuals showed the steepest tradeoff. Our extensive dataset in A. heterochaelis also included data about pairing, breeding season, and egg clutch size. Therefore, we could test for reproductive tradeoffs and benefits in this species. Female A. heterochaelis exhibited additional tradeoffs between weapon size and egg count, average egg volume, and total egg mass volume. For average egg volume, the smallest females exhibited the steepest tradeoff relative to weapon size. Furthermore, in males but not females, large weapons were positively correlated with the probability of being paired and the relative size of their pair mate. In conclusion, we establish that size-dependent tradeoffs underlie reliable scaling relationships of costly traits. Furthermore, we show that males and females differ in weapon investment, suggesting that weapons are especially beneficial to males and especially burdensome to females.

Section: Resultsmentioning

confidence: 99%

Tradeoffs explain scaling, sex differences, and seasonal oscillations in the remarkable weapons of snapping shrimp (Alpheus spp.)

2023

eLife

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“…Arrows represent behavioural transitions that occur more often than predicted if transitions were random, and arrow width represents transitional probabilities. with positive allometry (Dinh, 2022). Previous work has suggested that snapping shrimp shield their body from incoming snaps using their snapping claw, so positive allometry of claw exoskeleton could reflect scaling of defensive capacity (Herberholz & Schmitz, 1998).…”

Section: Discussionmentioning

confidence: 98%

“…Large mantis shrimp have thicker telsons, dissipate more energy and can withstand greater forces than small mantis shrimp (Taylor & Patek, 2010). In snapping shrimp, the exoskeleton of the weapon scales with positive allometry (Dinh, 2022). Previous work has suggested that snapping shrimp shield their body from incoming snaps using their snapping claw, so positive allometry of claw exoskeleton could reflect scaling of defensive capacity (Herberholz & Schmitz, 1998).…”

Section: Discussionmentioning

confidence: 99%

Weapon performance and contest assessment strategies of the cavitating snaps in snapping shrimp

2022

Functional Ecology

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Animals compete in contests over limited resources. Contestants forfeit once they ascertain that their opponent has greater resource‐holding potential (RHP; mutual assessment) or once they reach a threshold of costs (self‐assessment). Functional scaling studies of contest behaviour performance can inform how assessment signals, offensive capacity and endurance scale with RHP and thereby elucidate the mechanisms through which each of these assessment types operates. Here, we performed behavioural contest analyses to determine the assessment strategies used in snapping shrimp (Alpheus heterochaelis) contests. Then, we used biomechanical measurements of a common contest behaviour to inform how assessment might operate. We were specifically interested in the snapping behaviour during which snapping shrimp fire imploding cavitation bubbles—hereafter, ‘snaps’—at their opponents. We showed that A. heterochaelis use mutual assessment early in contests. Then, when they fire snaps, they switch to cumulative assessment—a type of self‐assessment where contestants endure costs from their own behaviours (e.g. energy) and their opponent's (e.g. injury). Because larger individuals tend to win contests, we then tested how the maximum performance and endurance of snaps scaled with size. We measured the average angular velocity of the snapping dactyl, cavitation bubble duration and pressure of snaps as metrics of performance. We measured 10 snaps per individual (n = 76 individuals). From this series of 10 snaps, we calculated the maximum of each metric as the maximum performance and the attrition of each metric over the course of 10 snaps as a measure of endurance. Maximum performance increased with size, but endurance did not. This suggests that cumulative assessment in snapping shrimp is driven by opponent‐imposed costs. Our results are not consistent with self‐assessment based on endurance; however, the experiment could not fully replicate the quick succession of snaps fired in real contests. Future experiments should better replicate the rapid firing of snaps to test if endurance matters in a more ecologically relevant context. Our framework of integrating biomechanics and behavioural ecology provides a pathway to identify precise mechanisms of contest assessment and animal behaviour more broadly. Read the free Plain Language Summary for this article on the Journal blog.

“…The proportion of the claw made of muscle decreases as weapon residual increases (Dinh, 2022). Therefore, we tested whether weapon residuals were negatively correlated with average angular velocity in the snapping claw, cavitation bubble duration, and snap pressure.…”

Section: Discussionmentioning

confidence: 99%

“…Larger weapons produce longer-lasting cavitation bubbles and greater pressures (Dinh & Patek, 2022). However, individuals that grow larger weapons than predicted by snapping claw scaling relationships do so using less muscle and more exoskeleton (Dinh, 2022). Reducing the amount of muscle in the claw may hinder elastic loading and snap production.…”

Section: Introductionmentioning

confidence: 99%

Tradeoffs and Benefits Explain Scaling, Sex Differences, and Seasonal Oscillations in the Remarkable Weapons of Snapping Shrimp (Alpheus spp.)

2022

Preprint

Self Cite

Evolutionary theory suggests that individuals should express costly traits at a magnitude that optimizes the cost-benefit ratio for the trait-bearer. Trait expression varies across a species because costs and benefits vary among individuals. For example, if large individuals pay lower costs than small individuals, then larger individuals should reach optimal cost-benefit ratios at a greater magnitude of trait expression. Using the remarkable cavitation-shooting weapons found in the big claws of male and female alpheid snapping shrimp, we test whether size- and sex-dependent expenditures explain the scaling of weapon size relative to body size and why males have larger proportional weapon size than females. We found that males and females from three snapping shrimp species (Alpheus heterochaelis, Alpheus angulosus, and Alpheus estuariensis) exhibit resource allocation tradeoffs between weapon and abdomen mass. For male A. heterochaelis, the species for which we had the greatest sample size and statistical power, the smallest individuals showed the steepest tradeoff. Our extensive dataset in A. heterochaelis also included data about pairing, breeding season, and egg clutch size. Therefore, we could test for reproductive tradeoffs and benefits in this species. Female A. heterochaelis exhibited additional tradeoffs between weapon size and egg count, average egg volume, and total egg mass volume. For average egg volume, the smallest females exhibited the steepest tradeoff relative to weapon size. Furthermore, for both sexes, large weapons were positively correlated with the relative size of their pair mate; however, for males only, large weapons were positively correlated with being paired in the first place. In conclusion, we establish that size-dependent tradeoffs underlie reliable scaling relationships of costly traits. Furthermore, we show that males and females differ in weapon investment, suggesting that weapons are especially beneficial to males and especially burdensome to females.