Male birds frequently face a trade‐off between acquiring mates and caring for offspring. Hormone manipulation studies indicate that testosterone often mediates this trade‐off, increasing mating ...effort while decreasing parental effort. Little is known, however, about individual covariation between testosterone and relevant behavior on which selection might act. Using wild, male dark‐eyed juncos (Junco hyemalis), we measured individual variation in testosterone levels before and after standardized injections of gonadotropin‐releasing hormone (GnRH). The GnRH challenges have been shown to produce short‐term testosterone increases that are similar to those produced naturally in response to social stimuli, repeatable in magnitude, and greater in males with more attractive ornaments. We correlated these testosterone increases with behavioral measures of mating and parental effort (aggressive response to a simulated territorial intrusion and nestling feeding, respectively). Males that showed higher postchallenge testosterone displayed more territorial behavior, and males that produced higher testosterone increases above initial levels displayed reduced parental behavior. Initial testosterone levels were positively but nonsignificantly correlated with aggression but did not predict parental behavior. These relationships suggest that natural variation in testosterone, specifically the production of short‐term increases, may underlie individual variation in the mating effort/parental effort trade‐off. We discuss the implications of these results for the evolution of hormonally mediated trade‐offs.
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Hormones mediate the expression of suites of correlated traits and hence may act both to facilitate and constrain adaptive evolution. Selection on one trait within a hormone-mediated suite may, for ...example, lead to a change in the strength of the hormone signal, causing either beneficial or detrimental changes in correlated traits. Theory and empirical methods for studying correlated trait evolution have been developed by the field of evolutionary quantitative genetics, and here we suggest that their application to the study of hormone-mediated suites may prove fruitful. We present hypotheses for how selection shapes the evolution of hormone-mediated suites and argue that correlational selection, which arises when traits interact in their effects on fitness, may act to alter or conserve the composition of hormone-mediated suites. Next, we advocate using quantitative genetic methods to assess natural covariation among hormone-mediated traits and to measure the strength of natural selection acting on them. Finally, we present illustrative examples from our own work on the evolution of testosterone-mediated suites in male and female dark-eyed juncos. We conclude that future work on hormone-mediated suites, if motivated by quantitative genetic theory, may provide important insights into their dual roles as adaptations and evolutionary constraints.
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The predictive power of genetic variation Uyeda, Josef C; McGlothlin, Joel W
Science (American Association for the Advancement of Science),
2024-May-10, 2024-05-10, 20240510, Volume:
384, Issue:
6696
Journal Article
Peer reviewed
New analyses show that trait variability links evolution across vastly different timescales.
Populations declining toward extinction can persist via genetic adaptation in a process called evolutionary rescue. Predicting evolutionary rescue has applications ranging from conservation biology ...to medicine, but requires understanding and integrating the multiple effects of a stressful environmental change on population processes. Here we derive a simple expression for how generation time, a key determinant of the rate of evolution, varies with population size during evolutionary rescue. Change in generation time is quantitatively predicted by comparing how intraspecific competition and the source of maladaptation each affect the rates of births and deaths in the population. Depending on the difference between two parameters quantifying these effects, the model predicts that populations may experience substantial changes in their rate of adaptation in both positive and negative directions, or adapt consistently despite severe stress. These predictions were then tested by comparison to the results of individual-based simulations of evolutionary rescue, which validated that the tolerable rate of environmental change varied considerably as described by analytical results. We discuss how these results inform efforts to understand wildlife disease and adaptation to climate change, evolution in managed populations and treatment resistance in pathogens.
Interactions among conspecifics influence social evolution through two distinct but intimately related paths. First, they provide the opportunity for indirect genetic effects (IGEs), where genes ...expressed in one individual influence the expression of traits in others. Second, interactions can generate social selection when traits expressed in one individual influence the fitness of others. Here, we present a quantitative genetic model of multivariate trait evolution that integrates the effects of both IGEs and social selection, which have previously been modeled independently. We show that social selection affects evolutionary change whenever the breeding value of one individual covaries with the phenotype of its social partners. This covariance can be created by both relatedness and IGEs, which are shown to have parallel roles in determining evolutionary response. We show that social selection is central to the estimation of inclusive fitness and derive a version of Hamilton's rule showing the symmetrical effects of relatedness and IGEs on the evolution of altruism. We illustrate the utility of our approach using altruism, greenbeards, aggression, and weapons as examples. Our model provides a general predictive equation for the evolution of social phenotypes that encompasses specific cases such as kin selection and reciprocity. The parameters can be measured empirically, and we emphasize the importance of considering both IGEs and social selection, in addition to relatedness, when testing hypotheses about social evolution.
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Abstract
Evolution by natural selection is often viewed as a process that inevitably leads to adaptation or an increase in population fitness over time. However, maladaptation, an evolved decrease in ...fitness, may also occur in response to natural selection under some conditions. Social selection, which arises from the effects of social partners on fitness, has been identified as a potential cause of maladaptation, but we lack a general rule identifying when social selection should lead to a decrease in population mean fitness. Here we use a quantitative genetic model to develop such a rule. We show that maladaptation is most likely to occur when social selection is strong relative to nonsocial selection and acts in an opposing direction. In this scenario, the evolution of traits that impose fitness costs on others may outweigh evolved gains in fitness for the individual, leading to a net decrease in population mean fitness. Furthermore, we find that maladaptation may also sometimes occur when phenotypes of interacting individuals negatively covary. We outline the biological situations where maladaptation in response to social selection can be expected, provide both quantitative genetic and phenotypic versions of our derived result, and suggest what empirical work would be needed to test it. We also consider the effect of social selection on inclusive fitness and support previous work showing that inclusive fitness cannot suffer an evolutionary decrease. Taken together, our results show that social selection may decrease population mean fitness when it opposes individual-level selection, even as inclusive fitness increases.
The evolution of sexual dimorphism is predicted to occur through reductions in between-sex genetic correlations (r
mf) for shared traits, but the physiological and genetic mechanisms that facilitate ...these reductions remain largely speculative. Here, we use a paternal half-sibling breeding design in captive brown anole lizards (Anolis sagrei) to show that the development of sexual size dimorphism is mirrored by the ontogenetic breakdown of r
mf for body size and growth rate. Using transcriptome data from the liver (which integrates growth and metabolism), we show that sex-biased gene expression also increases dramatically between ontogenetic stages bracketing this breakdown of r
mf. Ontogenetic increases in sex-biased expression are particularly evident for genes involved in growth, metabolism, and cell proliferation, suggesting that they contribute to both the development of sexual dimorphism and the breakdown of r
mf. Mechanistically, we show that treatment of females with testosterone stimulates the expression of male-biased genes while inhibiting the expression of female-biased genes, thereby inducing male-like phenotypes at both organismal and transcriptomic levels. Collectively, our results suggest that sex-specific modifiers such as testosterone can orchestrate sex-biased gene expression to facilitate the phenotypic development of sexual dimorphism while simultaneously reducing genetic correlations that would otherwise constrain the independent evolution of the sexes.
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Hormones coordinate the co-expression of behavioral, physiological, and morphological traits, giving rise to correlations among traits and organisms whose parts work well together. This article ...considers the implications of these hormonal correlations with respect to the evolution of hormone-mediated traits. Such traits can evolve owing to changes in hormone secretion, hormonal affinity for carrier proteins, rates of degradation and conversion, and interaction with target tissues to name a few. Critically, however, we know very little about whether these changes occur independently or in tandem, and thus whether hormones promote the evolution of tight phenotypic integration or readily allow the parts of the phenotype to evolve independently. For example, when selection favors a change in expression of hormonally mediated characters, is that alteration likely to come about through changes in hormone secretion (signal strength), changes in response to a fixed level of secretion (sensitivity of target tissues), or both? At one extreme, if the phenotype is tightly integrated and only the signal responds via selection's action on one or more hormonally mediated traits, adaptive modification may be constrained by past selection for phenotypic integration. Alternatively, response to selection may be facilitated if multivariate selection favors new combinations that can be easily achieved by a change in signal strength. On the other hand, if individual target tissues readily "unplug" from a hormone signal in response to selection, then the phenotype may be seen as a loose confederation that responds on a trait-by-trait basis, easily allowing adaptive modification, although perhaps more slowly than if signal variation were the primary mode of evolutionary response. Studies reviewed here and questions for future research address the relative importance of integration and independence by comparing sexes, individuals, and populations. Most attention is devoted to the hormone testosterone (T) and a songbird species, the dark-eyed junco (Junco hyemalis).
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Wondrously elaborate weapons and displays that appear to be counter to ecological optima are widespread features of male contests for mates across the animal kingdom. To understand how such diverse ...traits evolve, here we develop a quantitative genetic model of sexual selection for a male signaling trait that mediates aggression in male‐male contests and show that an honest indicator of aggression can generate selection on itself by altering the social environment. This can cause selection to accelerate as the trait is elaborated, leading to runaway evolution. Thus, an evolving source of selection provided by the social environment is the fundamental unifying feature of runaway sexual selection driven by either male‐male competition or female mate choice. However, a key difference is that runaway driven by male‐male competition requires signal honesty. Our model identifies simple conditions that provide clear, testable predictions for empirical studies using standard quantitative genetic methods.
Biologists and the public are captivated by extravagant traits used during male‐male contests for mates. Elaborations such as weapons, showy signals, and complex courtship are curious because they don't obviously contribute to survival, and in many instances would seem to work to attract predation. We provide a quantitative genetic model that shows how such elaboration can evolve, and when populations will shoot past an optimum leading to runaway evolution.
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Indirect genetic effects (IGEs), which occur when phenotypic expression in one individual is influenced by genes in another conspecific individual, may have a drastic effect on evolutionary response ...to selection. General evolutionary models of IGEs have been developed using two distinct theoretical frameworks derived from maternal effects theory. The first framework is trait-based and focuses on how phenotypes are influenced by specific traits in a social partner, with the strength of interactions defined by the matrix Ö. The second framework partitions total genetic variance into components representing direct effects, indirect effects, and the covariance between them, without identifying specific social traits responsible for IGEs. The latter framework has been employed more commonly by empiricists because the methods for estimating variance components are relatively straightforward. Here, we show how these two theoretical frameworks are related to each other and derive equations that can be used to translate between them. This translation leads to a generalized method that can be used to estimate Ψ via standard quantitative genetic breeding designs or pedigrees from natural populations. This method can be used in a very general set of circumstances and is widely applicable to all IGEs, including maternal effects and other interactions among relatives.
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