Tradeoffs explain scaling, sex differences, and seasonal oscillations in the remarkable weapons of snapping shrimp (Alpheus spp.)
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eLife assessment
This study on snapping shrimp morphological weaponry presents important findings on trade-offs in investment in costly weaponry traits as related to body size and reproduction. Convincing evidence is based on the collection of an exceptional number of fields samples, the inclusion of three shrimp species, and the measurement of numerous morphological and behavioral traits. The evidence shows that there are size-dependent trade-offs, where males and females differ in weapon investment, as weapons are beneficial to males but expensive for females. The findings will be of broad interest to evolutionary biologists and researchers working in the field of animal behavior.
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Abstract
Evolutionary theory suggests that individuals should express costly traits at a magnitude that optimizes the trait bearer’s cost-benefit difference. 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 greater trait magnitudes. Using the cavitation-shooting weapons found in the big claws of male and female snapping shrimp, we test whether size- and sex-dependent expenditures explain scaling and sex differences in weapon size. We found that males and females from three snapping shrimp species (Alpheus heterochaelis, Alpheus angulosus, and Alpheus estuariensis) show patterns consistent with tradeoffs between weapon and abdomen size. For male A. heterochaelis, the species for which we had the greatest statistical power, smaller individuals showed steeper tradeoffs. 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 tradeoffs between weapon size and egg count, average egg volume, and total egg mass volume. For average egg volume, smaller females exhibited steeper tradeoffs. Furthermore, in males but not females, large weapons were positively correlated with the probability of being paired and the relative size of their pair mates. In conclusion, we identified size-dependent tradeoffs that could underlie reliable scaling of costly traits. Furthermore, weapons are especially beneficial to males and burdensome to females, which could explain why males have larger weapons than females.
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eLife assessment
This study on snapping shrimp morphological weaponry presents important findings on trade-offs in investment in costly weaponry traits as related to body size and reproduction. Convincing evidence is based on the collection of an exceptional number of fields samples, the inclusion of three shrimp species, and the measurement of numerous morphological and behavioral traits. The evidence shows that there are size-dependent trade-offs, where males and females differ in weapon investment, as weapons are beneficial to males but expensive for females. The findings will be of broad interest to evolutionary biologists and researchers working in the field of animal behavior.
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Reviewer #1 (Public Review):
This research tackles an important question in evolutionary biology that has long stood on theory, with little experimental evidence to support this big idea. This paper provides a large natural dataset on several morphometric factors that allow a robust testing of the "handicap principle". The strength in this dataset comes from extensive field observations not only on morphology, but also fecundity and pairing behavior. The manuscript could use a little tightening up in prose, but the statistics and results are well explained. As the discussion mostly focuses on shrimp, generalizable principles are somewhat unclear. Overall, the research is an important finding that could one day be incorporated into undergraduate textbooks.
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Reviewer #2 (Public Review):
This study presents important findings on trade-offs in investment in costly traits related to survival and reproduction. The evidence supporting the claims of the authors is convincing with an exceptional sample size, the inclusion of three species, and measurement of numerous traits. The authors do not incorporate genetics or use experimentation, but they do use an elegant observational approach to glean the likely presence of trade-offs and improve understanding of investment in crucial life-history traits. The work will be of interest to evolutionary biologists, researchers working in the field of animal behavior, and those specializing in sexual selection.
The extent to which individuals should invest in costly traits is an ongoing puzzle to evolutionary biologists. Why is there a limit to investment in …
Reviewer #2 (Public Review):
This study presents important findings on trade-offs in investment in costly traits related to survival and reproduction. The evidence supporting the claims of the authors is convincing with an exceptional sample size, the inclusion of three species, and measurement of numerous traits. The authors do not incorporate genetics or use experimentation, but they do use an elegant observational approach to glean the likely presence of trade-offs and improve understanding of investment in crucial life-history traits. The work will be of interest to evolutionary biologists, researchers working in the field of animal behavior, and those specializing in sexual selection.
The extent to which individuals should invest in costly traits is an ongoing puzzle to evolutionary biologists. Why is there a limit to investment in traits that enhance survival or mating? Why do some individuals invest so much less than others in traits that should boost fitness? In this manuscript, Dinh and Patek use a strong sample size of snapping shrimp to investigate this question. They examine three species and measure numerous traits. The approach they use to deduce trade-offs is to examine residuals. Specifically, they plot the traits of interest against body size generating a regression for the population. Then, for each individual, they extract a residual value that is how much more or less they invest in a trait for a given body size. For example, some individuals might grow a big claw, but also express a small abdomen relative to others of the same size. The authors measure the extent to which each individual invests in a number of traits to investigate resource allocation trade-offs and reproductive benefits and costs.
This is an elegant and thorough study that thoughtfully examines how animals invest in their bodies and with what potential costs. They even look at male pairing success and the size of his mate to better understand the reproductive benefits of growing a larger claw in snapping shrimp. For females, they examine if growing a larger claw might lead to reduced reproduction because such females cannot care for as many eggs. The strengths of this study are many. It would, of course, be helpful to more thoroughly understand the costs and benefits of investment in claws, but the authors did an excellent job with what was possible. The current version of the manuscript would benefit from a discussion of the pros and cons of their approach of using residuals versus other approaches to measure resource allocation trade-offs.
Overall, this is such a nice study with excellent writing, and it will likely inspire others to examine trait investment in a myriad of other animals. It helps the field of sexual selection better understand the costs and benefits of growing a big (or small) weapon. And, more generally, it addresses the important question of why animals cannot have it all.
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