Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity.

Phenotypic plasticity is ubiquitous and generally regarded as a key mechanism for enabling organisms to survive in the face of environmental change. Because no organism is infinitely or ideally plastic, theory suggests that there must be limits (for example, the lack of ability to produce an optimal trait) to the evolution of phenotypic plasticity, or that plasticity may have inherent significant costs. Yet numerous experimental studies have not detected widespread costs. Explicitly differentiating plasticity costs from phenotype costs, we re-evaluate fundamental questions of the limits to the evolution of plasticity and of generalists vs specialists. We advocate for the view that relaxed selection and variable selection intensities are likely more important constraints to the evolution of plasticity than the costs of plasticity. Some forms of plasticity, such as learning, may be inherently costly. In addition, we examine opportunities to offset costs of phenotypes through ontogeny, amelioration of phenotypic costs across environments, and the condition-dependent hypothesis. We propose avenues of further inquiry in the limits of plasticity using new and classic methods of ecological parameterization, phylogenetics and omics in the context of answering questions on the constraints of plasticity. Given plasticity's key role in coping with environmental change, approaches spanning the spectrum from applied to basic will greatly enrich our understanding of the evolution of plasticity and resolve our understanding of limits.

Differential host susceptibility to Batrachochytrium dendrobatidis, an emerging amphibian pathogen.

The amphibian fungal pathogen Batrachochytrium dendrobatidis (Bd) has received considerable attention due to its role in amphibian population declines worldwide. Although many amphibian species appear to be affected by Bd, there is little information on species-specific differences in susceptibility to this pathogen. We used a comparative experimental approach to examine Bd susceptibility in 6 amphibian species from the United States. We exposed postmetamorphic animals to Bd for 30 days and monitored mortality, feeding rates, and infection levels. In all species tested, Bd-exposed animals had higher rates of mortality than unexposed (control) animals. However, we found differences in mortality rates among species even though the amount of Bd detected on the different species' bodies did not differ. Of the species tested, southern toads (Anaxyrus terrestris) and wood frogs (Lithobates sylvaticus) had the highest rates of Bd-related mortality. Within species, we detected lower levels of Bd on individuals that survived longer and found that the relationship between body size and infection levels differed among species. Our results indicate that, even under identical conditions, amphibian species differ in susceptibility to Bd. This study represents a step toward identifying and understanding species variation in disease susceptibility, which can be used to optimize conservation strategies.

Are there interactive effects of mate availability and predation risk on life history and defence in a simultaneous hermaphrodite?

Encountering mates and avoiding predators are ubiquitous challenges faced by many organisms and they can affect the expression of many traits including growth, timing of maturity and resource allocation to reproduction. However, these two factors are commonly considered in isolation rather than simultaneously. We examined whether predation risk and mate availability interact to affect morphology and life-history traits (including lifetime fecundity) of a hermaphroditic snail (Physa acuta). We found that mate availability reduced juvenile growth rate and final size. Predator cues from crayfish induced delayed reproduction, but there were no reduced fecundity costs associated with predator induction. Although there were interactive effects on longevity, lifetime fecundity was determined by the number of reproductive days. Therefore, our results indicate a resource-allocation trade-off among growth, longevity and reproduction. Future consideration of this interaction will be important for understanding how resource-allocation plasticity affects the integration of defensive, life-history and mating-system traits.

Effects of a common insecticide on wetland communities with varying quality of leaf litter inputs.

Chemical contamination of aquatic systems often co-occurs with dramatic changes in surrounding terrestrial vegetation. Plant leaf litter serves as a crucial resource input to many freshwater systems, and changes in litter species composition can alter the attributes of freshwater communities. However, little is known how variation in litter inputs interacts with chemical contaminants. We investigated the ecological effects resulting from changes in tree leaf litter inputs to freshwater communities, and how those changes might interact with the timing of insecticide contamination. Using the common insecticide malathion, we hypothesized that inputs of nutrient-rich and labile leaf litter (e.g., elm [Ulmus spp.] or maple [Acer spp.]) would reduce the negative effects of insecticides on wetland communities relative to inputs of recalcitrant litter (e.g., oak [Quercus spp.]). We exposed artificial wetland communities to a factorial combination of three litter species treatments (elm, maple, and oak) and four insecticide treatments (no insecticide, small weekly doses of 10 µg L-1, and either early or late large doses of 50 µg L-1). Communities consisted of microbes, algae, snails, amphipods, zooplankton, and two species of tadpoles. After two months, we found that maple and elm litter generally induced greater primary and secondary production. Insecticides induced a reduction in the abundance of amphipods and some zooplankton species, and increased phytoplankton. In addition, we found interactive effects of litter species and insecticide treatments on amphibian responses, although specific effects depended on application regime. Specifically, with the addition of insecticide, elm and maple litter induced a reduction in gray tree frog survival, oak and elm litter delayed tree frog metamorphosis, and oak and maple litter reduced green frog tadpole mass. Our results suggest that attention to local forest composition, as well as the timing of pesticide application might help ameliorate the harmful effects of pesticides observed in freshwater systems.

The heritability of inducible defenses in tadpoles.

The evolution of plastic traits requires phenotypic trade-offs and heritable traits, yet the latter requirement has received little attention, especially for predator-induced traits. Using a half-sib design, I examined the narrow-sense heritability of predator-induced behaviour, morphology, and life history in larval wood frogs (Rana sylvatica). Many of the traits had significant additive genetic variation in predator (caged Anax longipes) and no-predator environments. Whereas most traits had moderate to high heritability across environments, tail depth exhibited high heritability with predators but low heritability without predators. In addition, several traits had significant heritability for plasticity, suggesting a potential for selection to act on plasticity per se. Genetic correlations confirmed known phenotypic relationships across environments and identified novel relationships within each environment. This appears to be the first investigation of narrow-sense heritabilities for predator-induced traits and confirms that inducible traits previously shown to be under selection also have a genetic basis and should be capable of exhibiting evolutionary responses.

The lethal impacts of Roundup and predatory stress on six species of North American tadpoles.

The decline in amphibians across the globe has sparked a search for the causes, and recent evidence suggests a connection with pesticides. However, for most pesticides, tests on amphibians are rare and conducted only for short durations (1 to 4 days) and without natural stressors. Recent studies have discovered that the stress of predator cues in the water can make insecticides much more lethal to larval amphibians, but it is unknown whether this phenomenon can be generalized to other types of pesticides. Using six species of North American amphibian larvae (Rana sylvatica, R. pipiens, R. clamitans, R. catesbeiana, Bufo americanus, and Hyla versicolor), I examined the impact of a globally common herbicide (Roundup) on the survival of tadpoles for 16 days with and without the chemical cues emitted by predatory newts (Notophthalmus viridescens). LC50(16-d) estimates varied from 0.55 to 2.52 mg of active ingredient (AI)/L, which was considerably lower than the few previous studies using Roundup (1.5 to 15.5 mg AI/L). Moreover, in one of the six species tested (R. sylvatica), the addition of predatory stress made Roundup twice as lethal. This discovery suggests that synergistic interactions between predatory stress and pesticides may indeed be a generalizable phenomenon in amphibians that occurs with a wide variety of pesticides.

Predator-induced stress makes the pesticide carbaryl more deadly to gray treefrog tadpoles (Hyla versicolor).

Global declines in amphibians likely have multiple causes, including widespread pesticide use. Our knowledge of pesticide effects on amphibians is largely limited to short-term (4-d) toxicity tests conducted under highly artificial conditions to determine lethal concentrations (LC50). We found that if we used slightly longer exposure times (10-16 d), low concentrations of the pesticide carbaryl (3-4% of LC50(4-d)) killed 10-60% of gray treefrog (Hyla versicolor) tadpoles. If predatory cues also were present, the pesticide became 2-4 times more lethal, killing 60-98% of tadpoles. Thus, under more realistic conditions of increased exposure times and predatory stress, current application rates for carbaryl can potentially devastate gray treefrog populations. Further, because predator-induced stress is ubiquitous in animals and carbaryl's mode of action is common to many pesticides, these negative impacts may be widespread in nature.