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.

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.

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.

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 assessing the relative importance of predation and competition as agents of selection.

Field experiments that measure natural selection in response to manipulations of the selective regime are extremely rare, even in systems where the ecological basis of adaptation has been studied extensively. The adaptive radiation of Caribbean Anolis lizards has been studied for decades, leading to precise predictions about the influence of alternative agents of selection in the wild. Here we present experimental evidence for the relative importance of two putative agents of selection in shaping the adaptive landscape for a classic island radiation. We manipulated whole-island populations of the brown anole lizard, Anolis sagrei, to measure the relative importance of predation versus competition as agents of natural selection. We excluded or included bird and snake predators across six islands that ranged from low to high population densities of lizards, then measured subsequent differences in behaviour and natural selection in each population. Predators altered the lizards' perching behaviour and increased mortality, but predation treatments did not alter selection on phenotypic traits. By contrast, experimentally increasing population density dramatically increased the strength of viability selection favouring large body size, long relative limb length and high running stamina. Our results from A. sagrei are consistent with the hypothesis that intraspecific competition is more important than predation in shaping the selective landscape for traits central to the adaptive radiation of Anolis ecomorphs.

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.

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.

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.

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.

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.

Ocean currents mediate evolution in island lizards.

Islands are considered to be natural laboratories in which to examine evolution because of the implicit assumption that limited gene flow allows tests of evolutionary processes in isolated replicates. Here we show that this well-accepted idea requires re-examination. Island inundation during hurricanes can have devastating effects on lizard populations in the Bahamas. After severe storms, islands may be recolonized by over-water dispersal of lizards from neighbouring islands. High levels of gene flow may homogenize genes responsible for divergence, and are widely viewed as a constraining force on evolution. Ultimately, the magnitude of gene flow determines the extent to which populations diverge from one another, and whether or not they eventually form new species. We show that patterns of gene flow among island populations of Anolis lizards are best explained by prevailing ocean currents, and that over-water dispersal has evolutionary consequences. Across islands, divergence in fitness-related morphology decreases with increasing gene flow. Results suggest that over-water dispersal after hurricanes constrains adaptive diversification in Anolis lizards, and that it may have an important but previously undocumented role in this classical example of adaptive radiation.

Parallel shifts in ecology and natural selection in an island lizard.

BACKGROUND: Natural selection is a potent evolutionary force that shapes phenotypic variation to match ecological conditions. However, we know little about the year-to-year consistency of selection, or how inter-annual variation in ecology shapes adaptive landscapes and ultimately adaptive radiations. Here we combine remote sensing data, field experiments, and a four-year study of natural selection to show that changes in vegetation structure associated with a severe drought altered both habitat use and natural selection in the brown anole, Anolis sagrei. RESULTS: In natural populations, lizards increased their use of vegetation in wet years and this was correlated with selection on limb length but not body size. By contrast, a die-back of vegetation caused by drought was followed by reduced arboreality, selection on body size, and relaxed selection on limb length. With the return of the rains and recovery of vegetation, selection reverted back to pre-drought pattern of selection acting on limb length but not body size. To test for the impact of vegetation loss on natural selection during the drought, we experimentally removed vegetation on a separate study island in a naturally wet year. The experiment revealed similar inter-annual changes in selection on body size but not limb length. CONCLUSION: Our results illustrate the dynamic nature of ecology driving natural selection on Anolis morphology and emphasize the importance of inter-annual environmental variation in shaping adaptive variation. In addition, results illustrate the utility of using remote sensing data to examine ecology's role in driving natural selection.

Sexually antagonistic selection, sexual dimorphism, and the resolution of intralocus sexual conflict.

Males and females share most of their genomes and express many of the same traits, yet the sexes often have markedly different selective optima for these shared traits. This sexually antagonistic (SA) selection generates intralocus sexual conflict that is thought to be resolved through the evolution of sexual dimorphism. However, we currently know little about the prevalence of SA selection, the components of fitness that generate sexual antagonism, or the relationship between sexual dimorphism and current SA selection. We reviewed published studies to address these questions, using 424 selection estimates representing 89 traits from 34 species. Males and females often differed substantially in the direction and magnitude of selection on shared traits, although statistically significant SA selection was relatively uncommon. Sexual selection generated stronger sexual antagonism than fecundity or viability selection, and these individual components of fitness tended to reinforce one another to generate even stronger sexual antagonism for net fitness. Traits exhibiting strong sexual dimorphism exhibited greater SA selection than did weakly dimorphic traits, although this pattern was not significant after we controlled for the inclusion of multiple traits nested within species. Our results suggest that intralocus sexual conflict often may persist despite the evolution of sexual dimorphism.

Sex-specific adult dispersal and its selective consequences in the brown anole, Anolis sagrei.

1. Dispersal behaviour is a potentially risky life-history strategy that can impact habitat use as well as competition over territories and mates. 2. I studied natural selection on dispersal behaviour over the course of four breeding seasons in a Bahamian population of brown anoles (Anolis sagrei). 3. Both males and females showed extremely high site fidelity over the course of each reproductive season. Movement distance in males was negatively correlated with body size at first capture in spring (small males dispersed further). Moreover, differences in body size between dispersing males and the body size of the male territory residents that they replaced were correlated with the distance that males dispersed. Relatively larger males dispersed shorter distances compared with relatively smaller males. There was no relationship between dispersal distance and body size in females. However, females were more likely to disperse away from areas of low female density and into areas of higher female density, and female dispersal distances were negatively correlated with the number of female neighbours at the site of capture in spring (before dispersal). 4. These data suggest that, whereas male dispersal is driven by inter-male competition, female dispersal is more likely related to variation in territory quality. 5. Natural selection acted on dispersal distance in conjunction with male, but not female body size. Although smaller males were the more likely to disperse, these males paid a high cost in terms of viability indicating that dispersal is a potentially risky strategy.

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.

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.

Postcopulatory fertilization bias as a form of cryptic sexual selection.

Males and females share most of their genetic material yet often experience very different selection pressures. Some traits that are adaptive when expressed in males may therefore be maladaptive when expressed in females. Recent studies demonstrating negative correlations in fitness between parents and their opposite-sex progeny suggest that natural selection may favor a reduction in trait correlations between the sexes to partially mitigate intralocus sexual conflict. We studied sex-specific forms of selection acting in Anolis lizards in the Greater Antilles, a group for which the importance of natural selection has been well documented in species-level diversification, but for which less is known about sexual selection. Using the brown anole (Anolis sagrei), we measured fitness-related variation in morphology (body size), and variation in two traits reflecting whole animal physiological condition: running endurance and immune function. Correlations between body size and physiological traits were opposite between males and females and the form of natural selection acting on physiological traits significantly differed between the sexes. Moreover, physiological traits in progeny were correlated with the body-size of their sires, but correlations were null or even negative between parents and their opposite-sex progeny. Although results based on phenotypic and genetic correlations, as well as the action of natural selection, suggest the potential for intralocus sexual conflict, females used sire body size as a cue to sort sperm for the production of either sons or daughters. Our results suggest that intralocus sexual conflict may be at least partly resolved through post-copulatory sperm choice in A. sagrei.

Experimentally replicated disruptive selection on performance traits in a Caribbean lizard.

A central theme underlying studies of adaptive radiation is that ecologically mediated selection drives diversification. However, demonstrating the ecological basis of natural selection and linking this process to patterns of morphological diversity represents a formidable challenge. This is because selection experiments that test correlations between an organism's phenotype and its ecology are difficult to perform in the wild. Previous studies of Anolis lizards have shown that divergent morphologies are correlated with habitat use and have evolved repeatedly on islands throughout the Greater Antilles. Here, we show that the forms of selection acting within a species support an ecological mechanism for diversification. In natural populations, performance-related traits such as limb length are subject to correlational and disruptive selection driven by differences in habitat use. Experimental manipulations in the wild verify the same pattern of selection and indicate that both the targets and forms of selection are consistent through time. Elsewhere, we have demonstrated that these traits are heritable and should therefore evolve in response to selection. Our results provide evidence for the short-term repeatability of selection and its potency in the diversification of anoles.