Sex-specific heritabilities for length at maturity among Pacific salmonids and their consequences for evolution in response to artificial selection.

Artificial selection, whether intentional or coincidental, is a common result of conservation policies and natural resource management. To reduce unintended consequences of artificial selection, conservation practitioners must understand both artificial selection gradients on traits of interest and how those traits are correlated with others that may affect population growth and resilience. We investigate how artificial selection on male body size in Pacific salmon (Oncorhynchus spp.) may influence the evolution of female body size and female fitness. While salmon hatchery managers often assume that selection for large males will also produce large females, this may not be the case-in fact, because the fastest-growing males mature earliest and at the smallest size, and because female age at maturity varies little, small males may produce larger females if the genetic architecture of growth rate is the same in both sexes. We explored this possibility by estimating sex-specific heritability values of and natural and artificial selection gradients on length at maturity in four populations representing three species of Pacific salmon. We then used the multivariate breeder's equation to project how artificial selection against small males may affect the evolution of female length and fecundity. Our results indicate that the heritability of length at maturity is greater within than between the sexes and that sire-daughter heritability values are especially small. Salmon hatchery policies should consider these sex-specific quantitative genetic parameters to avoid potential unintended consequences of artificial selection.

Ecological rules for global species distribution also predict performance variation in Ironman triathletes.

Bergmann's and Allen's rules predict changes in body size and appendage length across temperature gradients for species with broad geographic distributions. Larger bodies and longer limbs facilitate cooling whereas smaller bodies and compact limbs limit heat loss. Although these patterns are highly repeatable (hence "rules" of ecology) the patterns and underlying mechanisms are less-well understood in humans. Here I show that variation in running performance among human male triathletes is consistent with both Bergmann's and Allen's rules. Males (but not females) with relatively larger body size and longer limbs performed better at hot compared to cold race venues and vice-versa. Consistent with results in other taxa, sex-specificity may reflect selection for sexual dimorphism. Results suggest that ecological patterns detected over large-spatial scales may arise from fine-scale variation in locomotor performance.

Individual contributions to group chorus dynamics influence access to mating opportunities in wood frogs.

A limitation in bioacoustic studies has been the inability to differentiate individual sonic contributions from group-level dynamics. We present a novel application of acoustic camera technology to investigate how individual wood frogs' calls influence chorus properties, and how variation influences mating opportunities. We recorded mating calls and used playback trials to gauge preference for different chorus types in the laboratory. Males and females preferred chorus playbacks with low variance in dominant frequency. Females preferred choruses with low mean peak frequency. Field studies revealed more egg masses laid in ponds where males chorused with low variance in dominant frequency. We also noted a trend towards more egg masses laid in ponds where males called with low mean frequency. Nearest-neighbour distances influenced call timing (neighbours called in succession) and distances increased with variance in chorus frequency. Results highlight the potential fitness implications of individual-level contributions to a bioacoustic signal produced by groups.

Reproductive trade-offs and phenotypic selection change with body condition, but not with predation regime, across island lizard populations.

Trade-offs between reproduction and survival are central to life-history theory and are expected to shape patterns of phenotypic selection, but the ecological factors structuring these trade-offs and resultant patterns of selection are generally unknown. We manipulated reproductive investment and predation regime in island populations of brown anole lizards (Anolis sagrei) to test (1) whether previously documented increases in the survival of experimentally non-reproductive females (OVX = ovariectomy) reflect the greater susceptibility of reproductive females (SHAM = control) to predation and (2) whether phenotypic selection differs as a function of reproductive investment and predation regime. OVX females exceeded SHAM controls in growth, mass gain and body condition, indicating pronounced energetic costs of reproduction. Although mortality was greatest in the presence of bird and snake predators, differences in survival between OVX and SHAM were unrelated to predation regime, as were patterns of natural selection on body size. Instead, we found that body condition at the conclusion of the experiment differed significantly across populations, suggesting that local environments varied in their ability to support mass gain and positive energy balance. As mean body condition improved across populations, the magnitude of the survival cost of reproduction increased, linear selection on body size shifted from positive to negative, and quadratic selection shifted from stabilizing to weakly disruptive. Our results suggest that reproductive trade-offs and patterns of phenotypic selection in female brown anoles are more sensitive to inferred variation in environmental quality than to experimentally induced variation in predation.

A potential role for restricted intertactical heritability in preventing intralocus conflict.

Intralocus sexual conflict, which arises when the same trait has different fitness optima in males and females, reduces population growth rates. Recently, evolutionary biologists have recognized that intralocus conflict can occur between morphs or reproductive tactics within a sex and that intralocus tactical conflict might constrain tactical dimorphism and population growth rates just as intralocus sexual conflict constrains sexual dimorphism and population growth rates. However, research has only recently focused on sexual and tactical intralocus conflict simultaneously, and there is no formal theory connecting the two. We present a graphical model of how tactical and sexual conflict over the same trait could constrain both sexual and tactical dimorphisms. We then use Coho salmon (Oncorhynchus kisutch), an important species currently protected under the Endangered Species Act, to investigate the possibility of simultaneous sexual and tactical conflict. Larger Coho males gain access to females through fighting while smaller males are favored through sneaking tactics, and female reproductive success is positively correlated with length. We tested for antagonistic selection on length at maturity among sexes and tactics and then used parent-offspring regression to calculate sex- and tactic-specific heritabilities to determine whether and where intralocus conflict exists. Selection on length varied in intensity and form among tactics and years. Length was heritable between dams and daughters (h 2 ± 95% CI = 0.361 ± 0.252) and between fighter males and their fighter sons (0.867 ± 0.312), but no other heritabilities differed significantly from zero. The lack of intertactical heritabilities in this system, combined with similar selection on length among tactics, suggests the absence of intralocus conflict between sexes and among tactics, allowing for the evolution of sexual and tactical dimorphisms. Our results suggest that Coho salmon populations are unlikely to be constrained by intralocus conflict or artificial selection on male tactic.

Experimental Evidence That Metamorphosis Alleviates Genomic Conflict.

Whenever genetically correlated traits experience antagonistic selection, an adaptive response in one trait can lead to a maladaptive response in the correlated trait. This is a form of genome-level conflict that can have important evolutionary consequences by impeding organisms from reaching their adaptive optima. Antagonistic selection should be pervasive in organisms with complex life histories because larval and adult life stages specialize in dramatically different environments. Since individuals express larval and adult morphologies from a single genome, genomic conflict across ontogenetic stages should also be prevalent. Using wood frogs as a study system, we measured natural selection on larval and postmetamorphic life stages and estimated genetic correlations among traits. Alternative life stages experienced a mix of both antagonistic and congruent viability selection. The integration between traits changed over the course of metamorphosis, reducing genetic correlations that cause conflict. Our results provide novel experimental evidence that metamorphosis can alleviate genomic conflict by partitioning life-history stages into modules that can more readily respond to selection. These results highlight the adaptive potential of metamorphosis as a means to avoid ecological specialization trade-offs. Moreover, they provide insights into the prevalence and evolutionary maintenance of complex life cycles.

Fitter frogs from polluted ponds: The complex impacts of human-altered environments.

Human-modified habitats rarely yield outcomes that are aligned with conservation ideals. Landscapes that are subdivided by roads are no exception, precipitating negative impacts on populations due to fragmentation, pollution, and road kill. Although many populations in human-modified habitats show evidence for local adaptation, rarely does environmental change yield outright benefits for populations of conservation interest. Contrary to expectations, we report surprising benefits experienced by amphibian populations breeding and dwelling in proximity to roads. We show that roadside populations of the wood frog, Rana sylvatica, exhibit better locomotor performance and higher measures of traits related to fitness compared with frogs from less disturbed environments located further away from roads. These results contrast previous evidence for maladaptation in roadside populations of wood frogs studied elsewhere. Our results indicate that altered habitats might not be unequivocally detrimental and at times might contribute to metapopulation success. While the frequency of such beneficial outcomes remains unknown, their occurrence underscores the complexity of inferring consequences of environmental change.

Survival of the Fastest: The Multivariate Optimization of Performance Phenotypes.

INTRODUCTION: Trade-offs are widespread in biological systems. Any investment in one trait must necessarily limit the investment in other traits. Still, many studies of physiological performance produce positive correlations between traits that are expected to trade-off with one another. Here we investigate why predicted trade-offs may often go unmeasured in studies of human athletes. METHODS: Triathletes compete in consecutive swimming, cycling, and running events as a single competition, events whose physical demands may be especially prone to generating performance trade-offs. Performance variation in these three events interacts to explain overall variation in athletic performance. RESULTS: We show that individual variation in athletic performance can mask trade-offs among disciplines, giving the impression that high-performance triathletes are athletic generalists. Covariance in race performance across the three disciplines was positive in the most elite athletes but became increasingly negative as race times increased. CONCLUSIONS: These performance trade-offs among the disciplines preclude the realization of a generalist athlete except in the most elite triathletes, a result similar to the "big houses, big cars" phenomenon in life history evolution. This distinction between trait combinations that are favored for optimal performance versus constrained by trade-offs was only apparent when accounting for individual level variation in athletic performance. Our results provide further evidence that meaningful trade-offs may be missed if individual variation in quality is disregarded.

Maternal allocation of carotenoids to eggs in an Anolis lizard.

The maternal allocation of carotenoids to eggs has been widely documented and manipulated. However, it is often assumed that the sole adaptive value of this allocation is to increase offspring fitness. Because carotenoids can be pro-oxidants or antioxidants depending on their concentrations and their chemical environment (i.e. presence of other antioxidants), dams may need to dispose of excess carotenoids upon depletion of other antioxidants to prevent oxidative damage. Additionally, the amount of carotenoids deposited in eggs may be dependent on male traits such as quality and coloration. We evaluated these two non-mutually exclusive hypotheses for carotenoid allocation to eggs and assessed paternal effects by supplementing male and female brown anole lizards, Anolis sagrei, with dietary carotenoids or with a combination of carotenoids and vitamin C. We found significant differences in the antioxidant capacities of fertilized and unfertilized eggs produced by female lizards, but the treatment did not affect the antioxidant capacity or carotenoid content of eggs. However, the carotenoid concentration of unfertilized eggs from carotenoid-supplemented females was significantly higher than eggs from the control group. Male coloration and body size did not affect the antioxidant capacity or carotenoid content of the eggs. Carotenoids may be allocated to unfertilized eggs to offset oxidative damage to the dam, with a neutral effect on offspring, rather than to solely provide antioxidant benefits to offspring as has been widely assumed.

A novel body coloration phenotype in Anolis sagrei: Implications for physiology, fitness, and predation.

In animals, color signals that convey information about quality are often associated with costs linked to the expression of coloration and may therefore be honest signals of sender quality. Honest indicators are often seen in sexual signals that are used by males to advertise quality to females. Carotenoid and pterin pigments are responsible for yellow, orange, and red coloration in a variety of taxa, but can also serve important roles as antioxidants by reducing free radicals in the body. In this study, we test the effects of a novel full-bodied orange color phenotype of the brown anole, Anolis sagrei, on mate choice, physiology, and survival. We found no evidence that lizards expressing the orange phenotype were preferred by females. Additionally, they did not differ in immune function, running endurance, or maximum sprint speed from lizards that did not express the novel phenotype. Pigment extractions revealed that orange body coloration resulted from pterin pigments and not carotenoids. Visual models suggest that the orange phenotype is less conspicuous to bird predators than the brown phenotype and may provide an adaptive explanation for the persistence of this trait. Given its small, yet positive effect on fitness, we expect the orange color phenotype to increase in frequency in subsequent decades.

Plasmodium Infections in Natural Populations of Anolis sagrei Reflect Tolerance Rather Than Susceptibility.

SYNOPSIS: Parasites can represent formidable selection pressures for hosts, but the cost of infection is sometimes difficult to demonstrate in natural populations. While parasite exploitation strategies may, in some instances, actually inflict low costs on their hosts, the response of hosts to infection is also likely to determine whether or not these costs can be detected. Indeed, costs of infection may be obscured if infected individuals in the wild are those that are the most tolerant, rather than the most susceptible, to infection. Here we test this hypothesis in two natural populations of Anolis sagrei, one of the most common anole lizard of the Bahamas. Plasmodium parasites were detected in > 7% of individuals and belonged to two distinct clades: P. mexicanum and P. floriensis. Infected individuals displayed greater body condition than non-infected ones and we found no association between infection status, stamina, and survival to the end of the breeding season. Furthermore, we found no significant difference in the immuno-competence (measured as a response to phytohemagglutinin challenge) of infected versus non-infected individuals. Taken together, our results suggest that the infected individuals that are caught in the wild are those most able to withstand the cost of the infection and that susceptible, infected individuals have been removed from the population (i.e., through disease-induced mortality). This study highlights the need for caution when interpreting estimates of infection costs in natural populations, as costs may appear low either when parasites exploitation strategies truly inflict low costs on their hosts or when those costs are so high that susceptible hosts are removed from the population.

The Ecology of Exercise: Mechanisms Underlying Individual Variation in Behavior, Activity, and Performance: An Introduction to Symposium.

SYNOPSIS: Wild animals often engage in intense physical activity while performing tasks vital for their survival and reproduction associated with foraging, avoiding predators, fighting, providing parental care, and migrating. In this theme issue we consider how viewing these tasks as "exercise"-analogous to that performed by human athletes-may help provide insight into the mechanisms underlying individual variation in these types of behaviors and the importance of physical activity in an ecological context. In this article and throughout this issue, we focus on four key questions relevant to the study of behavioral ecology that may be addressed by studying wild animal behavior from the perspective of exercise physiology: (1) How hard do individual animals work in response to ecological (or evolutionary) demands?; (2) Do lab-based studies of activity provide good models for understanding activity in free-living animals and individual variation in traits?; (3) Can animals work too hard during "routine" activities?; and (4) Can paradigms of "exercise" and "training" be applied to free-living animals? Attempts to address these issues are currently being facilitated by rapid technological developments associated with physiological measurements and the remote tracking of wild animals, to provide mechanistic insights into the behavior of free-ranging animals at spatial and temporal scales that were previously impossible. We further suggest that viewing the behaviors of non-human animals in terms of the physical exercise performed will allow us to fully take advantage of these technological advances, draw from knowledge and conceptual frameworks already in use by human exercise physiologists, and identify key traits that constrain performance and generate variation in performance among individuals. It is our hope that, by highlighting mechanisms of behavior and performance, the articles in this issue will spur on further synergies between physiologists and ecologists, to take advantage of emerging cross-disciplinary perspectives and technologies.

Performance Tradeoffs, Ontogenetic Conflict, and Multisport Athletes: How is an Ironman Triathlete Like a Frog?

SYNOPSIS: Life-history theory is a cornerstone of modern evolutionary biology that addresses myriad phenomena ranging from demography and population structure to the evolution of aging and senescence. Trade-offs may arise in a number of contexts, from allocation-based (e.g., egg size vs. egg number) to genomic conflicts (e.g., intralocus sexual conflict in which genes that perform well in males perform poorly in females). Here we test for performance tradeoffs in human athletes. We show that in Ironman triathletes, swimming performance trades off with cycling and running performance. The tradeoff appears to be plastic, in that only highly trained athletes experience the tradeoff. We then investigate whether wood frogs (Rana sylvatica) experience similar locomotor performance tradeoffs, to ask whether the divergent environments experienced by tadpoles and frogs leads to ontogenetic conflict (tradeoffs over development). We show that although swimming and jumping performance are positively correlated, antagonistic natural selection may still favor alternative adaptive optima in the two life history stages. However, "adaptive decoupling" of the life stages during metamorphosis may resolve ontogenetic conflict and facilitate independent adaptation to both environments. Thus, whereas performance tradeoffs are general in both systems, the unique selective environment of amphibians has favored the evolution of mechanisms to alleviate the costs of those tradeoffs.

Spatial variation in climate mediates gene flow across an island archipelago.

High levels of gene flow among partially isolated populations can overwhelm selection and limit local adaptation. This process, known as "gene swamping," can homogenize genetic diversity among populations and reduce the capacity of a species to withstand rapid environmental change. We studied brown anole lizards (Anolis sagrei) distributed across seven islands in The Bahamas. We used microsatellite markers to estimate gene flow among islands and then examined the correlation between thermal performance and island temperature. The thermal optimum for sprint performance was correlated with both mean and maximum island temperature, whereas performance breadth was not correlated with any measure of temperature variation. Gene flow between islands decreased as the difference between mean island temperatures increased, even when those islands were adjacent to one another. These data suggest that phenotypic variation is the result of either (1) local genetic adaptation with selection against immigrants maintaining variation in the thermal optimum, (2) irreversible forms of adaptive plasticity such that immigrants have reduced fitness, or (3) an interaction between fixed genetic differences and plasticity. In general, the patterns of gene flow we observed suggest that local thermal environments represent important ecological filters that can mediate gene flow on relatively fine geographic scales.

Field estimates of parentage reveal sexually antagonistic selection on body size in a population of Anolis lizards.

Sexual dimorphism evolves when selection favors different phenotypic optima between the sexes. Such sexually antagonistic selection creates intralocus sexual conflict when traits are genetically correlated between the sexes and have sex-specific optima. Brown anoles are highly sexually dimorphic: Males are on average 30% longer than females and 150% heavier in our study population. Viability selection on body size is known to be sexually antagonistic, and directional selection favors large male size whereas stabilizing selection constrains females to remain small. We build on previous studies of viability selection by measuring sexually antagonistic selection using reproductive components of fitness over three generations in a natural population of brown anoles. We estimated the number of offspring produced by an individual that survived to sexual maturity (termed RSV), a measure of individual fitness that includes aspects of both individual reproductive success and offspring survival. We found directional selection on male body size, consistent with previous studies of viability selection. However, selection on female body size varied among years, and included periods of positive directional selection, quadratic stabilizing selection, and no selection. Selection acts differently in the sexes based on both survival and reproduction and sexual conflict appears to be a persistent force in this species.

Natural selection on thermal performance in a novel thermal environment.

Tropical ectotherms are thought to be especially vulnerable to climate change because they are adapted to relatively stable temperature regimes, such that even small increases in environmental temperature may lead to large decreases in physiological performance. One way in which tropical organisms may mitigate the detrimental effects of warming is through evolutionary change in thermal physiology. The speed and magnitude of this response depend, in part, on the strength of climate-driven selection. However, many ectotherms use behavioral adjustments to maintain preferred body temperatures in the face of environmental variation. These behaviors may shelter individuals from natural selection, preventing evolutionary adaptation to changing conditions. Here, we mimic the effects of climate change by experimentally transplanting a population of Anolis sagrei lizards to a novel thermal environment. Transplanted lizards experienced warmer and more thermally variable conditions, which resulted in strong directional selection on thermal performance traits. These same traits were not under selection in a reference population studied in a less thermally stressful environment. Our results indicate that climate change can exert strong natural selection on tropical ectotherms, despite their ability to thermoregulate behaviorally. To the extent that thermal performance traits are heritable, populations may be capable of rapid adaptation to anthropogenic warming.

Experimentally decoupling reproductive investment from energy storage to test the functional basis of a life-history trade-off.

The ubiquitous life-history trade-off between reproduction and survival has long been hypothesized to reflect underlying energy-allocation trade-offs between reproductive investment and processes related to self-maintenance. Although recent work has questioned whether energy-allocation models provide sufficient explanations for the survival cost of reproduction, direct tests of this hypothesis are rare, especially in wild populations. This hypothesis was tested in a wild population of brown anole lizards (Anolis sagrei) using a two-step experiment. First, stepwise variation in reproductive investment was created using unilateral and bilateral ovariectomy (OVX) along with intact (SHAM) control. Next, this manipulation was decoupled from its downstream effects on energy storage by surgically ablating the abdominal fat stores from half of the females in each reproductive treatment. As predicted, unilateral OVX (intermediate reproductive investment) induced levels of growth, body condition, fat storage and breeding-season survival that were intermediate between the high levels of bilateral OVX (no reproductive investment) and the low levels of SHAM (full reproductive investment). Ablation of abdominal fat bodies had a strong and persistent effect on energy stores, but it did not influence post-breeding survival in any of the three reproductive treatments. This suggests that the energetic savings of reduced reproductive investment do not directly enhance post-breeding survival, with the caveat that only one aspect of energy storage was manipulated and OVX itself had no overall effect on post-breeding survival. This study supports the emerging view that simple energy-allocation models may often be insufficient as explanations for the life-history trade-off between reproduction and survival.

The impact of climate change measured at relevant spatial scales: new hope for tropical lizards.

Much attention has been given to recent predictions that widespread extinctions of tropical ectotherms, and tropical forest lizards in particular, will result from anthropogenic climate change. Most of these predictions, however, are based on environmental temperature data measured at a maximum resolution of 1 km(2), whereas individuals of most species experience thermal variation on a much finer scale. To address this disconnect, we combined thermal performance curves for five populations of Anolis lizard from the Bay Islands of Honduras with high-resolution temperature distributions generated from physical models. Previous research has suggested that open-habitat species are likely to invade forest habitat and drive forest species to extinction. We test this hypothesis, and compare the vulnerabilities of closely related, but allopatric, forest species. Our data suggest that the open-habitat populations we studied will not invade forest habitat and may actually benefit from predicted warming for many decades. Conversely, one of the forest species we studied should experience reduced activity time as a result of warming, while two others are unlikely to experience a significant decline in performance. Our results suggest that global-scale predictions generated using low-resolution temperature data may overestimate the vulnerability of many tropical ectotherms to climate change.

Predator mediated selection and the impact of developmental stage on viability in wood frog tadpoles (Rana sylvatica).

BACKGROUND: Complex life histories require adaptation of a single organism for multiple ecological niches. Transitions between life stages, however, may expose individuals to an increased risk of mortality, as the process of metamorphosis typically includes developmental stages that function relatively poorly in both the pre- and post-metamorphic habitat. We studied predator-mediated selection on tadpoles of the wood frog, Rana sylvatica, to identify this hypothesized period of differential predation risk and estimate its ontogenetic onset. We reared tadpoles in replicated mesocosms in the presence of the larval odonate Anax junius, a known tadpole predator. RESULTS: The probability of tadpole survival increased with increasing age and size, but declined steeply at the point in development where hind limbs began to erupt from the body wall. Selection gradient analyses indicate that natural selection favored tadpoles with short, deep tail fins. Tadpoles resorb their tails as they progress toward metamorphosis, which may have led to the observed decrease in survivorship. Path models revealed that selection acted directly on tail morphology, rather than through its indirect influence on swimming performance. CONCLUSIONS: This is consistent with the hypothesis that tail morphology influences predation rates by reducing the probability a predator strikes the head or body.

Paternal condition drives progeny sex-ratio bias in a lizard that lacks parental care.

Sex-allocation theory predicts that females in good condition should preferentially produce offspring of the sex that benefits the most from an increase in maternal investment. However, it is generally assumed that the condition of the sire has little effect on progeny sex ratio, particularly in species that lack parental care. We used a controlled breeding experiment and molecular paternity analyses to examine the effects of both maternal and paternal condition on progeny sex ratio and progeny fitness in the brown anole (Anolis sagrei), a polygynous lizard that lacks parental care. Contrary to the predictions of sex-allocation theory, we found no relationship between maternal condition and progeny sex ratio. By contrast, progeny sex ratio shifted dramatically from female-biased to male-biased as paternal condition increased. This pattern was driven entirely by an increase in the production of sons as paternal condition improved. Despite strong natural selection favoring large size and high condition in both sons and daughters, we found no evidence that progeny survival was related to paternal condition. Our results emphasize the importance of considering the paternal phenotype in studies of sex allocation and highlight the need for further research into the pathways that link paternal condition to progeny fitness.