An official website of the United States government
Synopsis Sexual selection drives the evolution of a broad diversity of traits, such as the enlarged claws of fiddler crabs, the high-energy behavioral displays of hummingbirds, the bright red plumage of house finches, the elaborated antennae of moths, the wing “snapping” displays of manakins and the calculated calls of túngara frogs. A majority of work in sexual selection has aimed to measure the magnitude of these traits. Yet, we know surprisingly little about the physiology shaping such a diversity of sexually selected behavior and supportive morphology. The energetic properties underlying sexual signals are ultimately fueled by metabolic machinery at multiple scales, from mitochondrial properties and enzymatic activity to hormonal regulation and the modification of muscular and neural tissues. However, different organisms have different physiological constraints and face various ecological selection pressures; thus, selection operates and interacts at multiple scales to shape sexually selected traits and behavior. In this perspective piece, we describe illustrative case studies in different organisms to emphasize that understanding the physiological and energetic mechanisms that shape sexual traits may be critical to understanding their evolution and ramifications with ecological selection. We discuss (1) the way sexual selection shapes multiple integrated components of physiology, behavior, and morphology, (2) the way that sexually selected carotenoid pigments may reflect some aspects of cellular processes, (3) the relationship between sexually selected modalities and energetics, (4) the hormone ecdysone and its role in shaping sex-specific phenotypes in insects, (5) the way varied interaction patterns and social contexts select for signaling strategies that are responsive to social scenes, and (6) the role that sexual selection may have in the exploitation of novel thermal niches. Our major objective is to describe how sexually selected behavior, physiology, and ecology are shaped in diverse organisms so that we may develop a deeper and more integrated understanding of sexual trait evolution and its ecological consequences.
more »
« less
Predation drives complex eco-evolutionary dynamics in sexually selected traits
Predation plays a role in preventing the evolution of ever more complicated sexual displays, because such displays often increase an individual’s predation risk. Sexual selection theory, however, omits a key feature of predation in modeling costs to sexually selected traits: Predation is density dependent. As a result of this density dependence, predator–prey dynamics should feed back into the evolution of sexual displays, which, in turn, feeds back into predator–prey dynamics. Here, we develop both population and quantitative genetic models of sexual selection that explicitly link the evolution of sexual displays with predator–prey dynamics. Our primary result is that predation can drive eco-evolutionary cycles in sexually selected traits. We also show that mechanistically modeling the cost to sexual displays as predation leads to novel outcomes such as the maintenance of polymorphism in sexual displays and alters ecological dynamics by muting prey cycles. These results suggest predation as a potential mechanism to maintain variation in sexual displays and underscore that short-term studies of sexual display evolution may not accurately predict long-run dynamics. Further, they demonstrate that a common verbal model (that predation limits sexual displays) with widespread empirical support can result in unappreciated, complex dynamics due to the density-dependent nature of predation.
more »
« less
- Award ID(s):
- 1939290
- PAR ID:
- 10503172
- Editor(s):
- Patricelli, Gail L.
- Publisher / Repository:
- PLoS
- Date Published:
- Journal Name:
- PLOS Biology
- Volume:
- 21
- Issue:
- 4
- ISSN:
- 1545-7885
- Page Range / eLocation ID:
- e3002059
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract The healthy herds hypothesis proposes that predators can reduce parasite prevalence and thereby increase the density of their prey. However, evidence for such predator‐driven reductions in the prevalence of prey remains mixed. Furthermore, even less evidence supports increases in prey density during epidemics. Here, we used a planktonic predator–prey–parasite system to experimentally test the healthy herds hypothesis. We manipulated density of a predator (the phantom midge, Chaoborus punctipennis ) and parasitism (the virulent fungus Metschnikowia bicuspidata ) in experimental assemblages. Because we know natural populations of the prey ( Daphnia dentifera ) vary in susceptibility to both predator and parasite, we stocked experimental populations with nine genotypes spanning a broad range of susceptibility to both enemies. Predation significantly reduced infection prevalence, eliminating infection at the highest predation level. However, lower parasitism did not increase densities of prey; instead, prey density decreased substantially at the highest predation levels (a major density cost of healthy herds predation). This density result was predicted by a model parameterized for this system. The model specifies three conditions for predation to increase prey density during epidemics: (i) predators selectively feed on infected prey, (ii) consumed infected prey release fewer infectious propagules than unconsumed prey, and (iii) sufficiently low infection prevalence. While the system satisfied the first two conditions, prevalence remained too high to see an increase in prey density with predation. Low prey densities caused by high predation drove increases in algal resources of the prey, fueling greater reproduction, indicating that consumer–resource interactions can complicate predator–prey–parasite dynamics. Overall, in our experiment, predation reduced the prevalence of a virulent parasite but, at the highest levels, also reduced prey density. Hence, while healthy herds predation is possible under some conditions, our empirical results make it clear that the manipulation of predators to reduce parasite prevalence may harm prey density.more » « less
-
Abstract Invasive predatory species are frequently observed to cause evolutionary responses in prey phenotypes, which in turn may lead to evolutionary shifts in the population dynamics of prey. Research has provided a link between rates of predation and the evolution of prey population growth in the lab, but studies from natural populations are rare. Here, we tested for evolutionary changes in population dynamics parameters of zooplanktonDaphnia pulicariafollowing invasion by the predatorBythotrephes longimanusinto Lake Kegonsa, Wisconsin, US. We used a resurrection ecological approach, whereby clones from pre‐ and post‐invasive periods were hatched from eggs obtained in sediment cores and were used in a 3‐month growth experiment. Based on these data, we estimated intrinsic population growth rates (r), the shape of density dependence (θ) and carrying capacities (K) using theta‐logistic models. We found that post‐invasionDaphniamaintained a higherrandKunder these controlled, predation‐free laboratory conditions. Evidence for changes inθwas weaker. Whereas previous experimental evolution studies of predator–prey interactions have demonstrated that genotypes that have evolved under predation have inferior competitive ability when the predator is absent, this was not the case for theDaphnia. Given that our study was conducted in a laboratory environment and the possibility for genotype‐by‐environment interactions, extrapolating these apparent counterintuitive results to the wild should be done with caution. However, barring such complications, we discuss how selection for reduced predator exposure, either temporally or spatially, may have led to the observed changes. This scenario suggests that complexities in ecological interactions represents a challenge when predicting the evolutionary responses of population dynamics to changes in predation pressure in natural systems.more » « less
-
Abstract Predator and prey traits are important determinants of the outcomes of trophic interactions. In turn, the outcomes of trophic interactions shape predator and prey trait evolution. How species' traits respond to selection from trophic interactions depends crucially on whether and how heritable species' traits are and their genetic correlations. Of the many traits influencing the outcomes of trophic interactions, body size and movement traits have emerged as key traits. Yet, how these traits shape and are shaped by trophic interactions is unclear, as few studies have simultaneously measured the impacts of these traits on the outcomes of trophic interactions, their heritability, and their correlations within the same system.We used outcrossed lines of the ciliate protistParamecium caudatumfrom natural populations to examine variation in morphology and movement behaviour, the heritability of that variation, and its effects onParameciumsusceptibility to predation by the copepodMacrocyclops albidus.We found that theParameciumlines exhibited heritable variation in body size and movement traits. In contrast to expectations from allometric relationships, body size and movement speed showed little covariance among clonal lines. The proportion ofParameciumconsumed by copepods was positively associated withParameciumbody size and velocity but with an interaction such that greater velocities led to greater predation risk for large body‐sized paramecia but did not alter predation risk for smaller paramecia. The proportion of paramecia consumed was not related to copepod body size. These patterns of predation risk and heritable trait variation in paramecia suggest that copepod predation may act as a selective force operating independently on movement and body size and generating the strongest selection against large, high‐velocity paramecia.Our results illustrate how ecology and genetics can shape potential natural selection on prey traits through the outcomes of trophic interactions. Further simultaneous measures of predation outcomes, traits, and their quantitative genetics will provide insights into the evolutionary ecology of species interactions and their eco‐evolutionary consequences. Read the freePlain Language Summaryfor this article on the Journal blog.more » « less
-
A morphological trait can have multiple functions shaped by varying selective forces. Bare parts in birds, such as wattles, casques and combs, are known to function in both signalling and thermoregulation. Studies have demonstrated such structures are targets of sexual selection via female choice in several species of Galliformes (junglefowl, turkeys and grouse), though other studies have shown some role in thermoregulation (guineafowl). Here, we tested fundamental hypotheses regarding the evolution and maintenance of bare parts in Galliformes. Using a phylogeny that included nearly 90% of species in the order, we evaluated the role of both sexual and natural selection in shaping the function of bare parts across different clades. We found a combination of both environmental and putative sexually selected traits strongly predicted the variation of bare parts for both males and females across Galliformes. When the analysis is restricted to the largest family, Phasianidae (pheasants, junglefowl and allies), sexually selected traits were the primary predictors of bare parts. Our results suggest that bare parts are important for both thermoregulation and sexual signalling across Galliformes but are primarily under strong sexual selection within the Phasianidae.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript
- Journal Article:
- https://doi.org/10.1371/journal.pbio.3002059
