NATURAL SELECTION FOR ENVIRONMENTALLY INDUCED PHENOTYPES IN TADPOLES

Models suggest that phenotypic plasticity is maintained in situations where the optimal phenotype differs through time or space, so that selection acts in different directions in different environments. Some empirical work supports the general premise of this prediction because phenotypes induced by a particular environment sometimes perform better than other phenotypes when tested in that environment. We have extended these results by estimating the targets of selection in Pseudacris triseriata tadpoles in environments without predators and with larval Anax dragonflies. Tadpoles displayed significant behavioral and morphological plasticity when reared in the presence and absence of nonlethal dragonflies for 32 days in cattle tanks. We measured selection in the absence of free predators by regressing growth and survival in the tanks against activity and several measures of tail and body shape. We measured selection in the presence of predators by exposing groups of 10 tadpoles to Anax in overnight predation trials and regressing the average phenotype of survivors against the number of tadpoles killed. Selection in the two environments acted in opposite directions on both tail and body shape, although the affected fitness components were different. In the presence of Anax, tadpoles with shallow and narrow body, deep tail fin, and wide tail muscle survived best. In the absence of free predators, tadpoles with narrow tail muscle grew significantly faster, and those with shallow tail fin and deep body grew somewhat faster. Activity was unrelated to survival or growth in either environment. Developmental plasticity in tail shape closely paralleled selection, because tail fin depth increased after long-term exposure to Anax and tail muscle width tended to increase. In contrast, there was no plasticity in body shape in spite of strong selection for decreasing body depth. Thus, when confronted with a dragonfly predator, P. triseriata tadpoles adjusted their tail shape (but not body shape) almost exactly in the direction of selection imposed by Anax. These results suggest that phenotypic plasticity in some morphological traits, such as tail depth and tail muscle width, has evolved under intermittent selection by dragonflies. Other traits that undergo selection by dragonflies, such as body morphology, appear developmentally rigid, perhaps because of historically strong opposing selection in nature or other constraints.     

Functional mechanisms of an inducible defence in tadpoles: morphology and behaviour influence mortality risk from predation

In many amphibian larvae a suite of morphological and behavioural characters varies together in an induced defence against predators, but it remains unclear which features are functionally related to defence. We independently manipulated behaviour and morphology in tadpoles of Hyla versicolor and assessed their consequences for swimming performance and predator escape. Data on burst swimming showed that tadpoles which accelerated rapidly were elongate, with shallow bodies and tails. Predator escape was measured by exposing tadpoles to predators (larval Anax dragonflies or larval Ambystoma salamanders) and recording time until death. Tadpoles were first reared for 30 days in ponds containing either caged Anax or no predators; individuals responded to predators by developing large brightly coloured tails and short bodies. We placed tadpoles of both morphological phenotypes into plastic tubs, and manipulated their behaviour using food and chemical cues from predators. Mortality risk experienced by the predator‐induced phenotype was about half that of the no‐predator phenotype, and risk increased with time spent swimming. An interaction between morphology and behaviour arose because increasing activity caused higher risk for tadpoles with deep tail fins but not shallow tail fins.     

Naturally occurring variation in tadpole morphology and performance linked to predator regime

Divergent natural selection drives a considerable amount of the phenotypic and genetic variation observed in natural populations. For example, variation in the predator community can generate conflicting selection on behavioral, life‐history, morphological, and performance traits. Differences in predator regime can subsequently increase phenotypic and genetic variations in the population and result in the evolution of reproductive barriers (ecological speciation) or phenotypic plasticity. We evaluated morphology and swimming performance in field collected Bronze Frog larvae (Lithobates clamitans) in ponds dominated by predatory fish and those dominated by invertebrate predators. Based on previous experimental findings, we hypothesized that tadpoles from fish‐dominated ponds would have small bodies, long tails, and large tail muscles and that these features would facilitate fast‐start speed. We also expected to see increased tail fin depth (i.e., the tail‐lure morphology) in tadpoles from invertebrate‐dominated ponds. Our results support our expectations with respect to morphology in affecting swimming performance of tadpoles in fish‐dominated ponds. Furthermore, it is likely that divergent natural selection is playing a role in the diversification on morphology and locomotor performance in this system.     

Predator‐induced phenotypic plasticity in tadpoles: extension or innovation?

Phenotypic plasticity, the ability of a trait to change as a function of the environment, is central to many ideas in evolutionary biology. A special case of phenotypic plasticity observed in many organisms is mediated by their natural predators. Here, we used a predator-prey system of dragonfly larvae and tadpoles to determine if predator-mediated phenotypic plasticity provides a novel way of surviving in the presence of predators (an innovation) or if it represents a simple extension of the way noninduced tadpoles survive predation. Tadpoles of Limnodynastes peronii were raised in the presence and absence of predation, which then entered a survival experiment. Induced morphological traits, primarily tail height and tail muscle height, were found to be under selection, indicating that predator-mediated phenotypic plasticity may be adaptive. Although predator-induced animals survived better, the multivariate linear selection gradients were similar between the two tadpole groups, suggesting that predator-mediated phenotypic plasticity is an extension of existing survival strategies. In addition, nonlinear selection gradients indicated a cost of predator-induced plasticity that may limit the ability of phenotypic plasticity to enhance survival in the presence of predators.     

Spatially heterogeneous selection in nature favors phenotypic plasticity in anuran larvae

Theory holds that adaptive phenotypic plasticity evolves under spatial or temporal variation in natural selection. I tested this prediction in a classic system of predator‐induced plasticity: frog tadpoles (Rana temporaria) reacting to predaceous aquatic insects. An outdoor mesocosm experiment manipulating exposure to Aeshna dragonfly larvae revealed plasticity in most characters: growth, development, behavior, and external morphology. I measured selection by placing 1927 tadpoles into enclosures within natural ponds; photographs permitted identification of the survivors six to nine days later. Fitness was defined as a linear combination of growth, development, and survival that correlates with survival to age 2 in another anuran species. In enclosures with many predators, selection‐favored character values similar to those induced by exposure to Aeshna in mesocosms. The shift in selection along the predation gradient was strongest for characters that exhibited high predator‐induced plasticity. A field survey of 50 ponds revealed that predator density changes over a spatial scale relevant for movement of individual adults and larvae: 17% of variation in predation risk was among ponds separated by tens to thousands of meters and 81% was among sites ≤10 m apart within ponds. These results on heterogeneity in the selection regime confirm a key tenant of the standard model for the evolution of plasticity.     

Microgeographic adaptations of spotted salamander morphological defenses in response to a predaceous salamander and beetle

Spatial heterogeneity in the selection imposed by different predator species could promote the adaptive diversification of local prey populations. However, high gene flow might swamp local adaptations at limited spatial scales or generalized phenotypic plasticity might evolve in place of local diversification. Spotted salamander larvae Ambystoma maculatum face strongly varying risks from gape‐limited marbled salamander larvae Ambystoma opacum and gape‐unconstrained diving beetle larvae Dytiscus spp. across natural landscapes. To evaluate if A. maculatum adapts to these predation risk across micro‐geographic scales, I measured selection gradients in response to the two focal predators and then assayed the defensive morphologies of ten populations in a common garden experiment. I found that A. opacum induced selection on A. maculatum for larger tailfins and bodies whereas beetles induced selection for larger tail muscles and smaller bodies. In accordance with the local adaptation hypothesis, A. maculatum populations inhabiting ponds with high beetle densities grew larger tail muscles relative to other populations when raised in a common environment. However, populations exposed to strong A. opacum selection did not evolve larger tailfins as predicted. High gene flow or morphological plasticity could explain the absence of this morphological response to A. opacum. Overall, results suggest that populations can sometimes evolve adaptive traits in response to locally variable selection regimes even across the very limited distances that separate populations in this study. If prey populations often differ in their defenses against local predators, then this variation could affect the outcome of species interactions in local communities.     

COSTS AND BENEFITS OF A PREDATOR-INDUCED POLYPHENISM IN THE GRAY TREEFROG HYLA CHRYSOSCELIS

The phenotypes of gray treefrog (Hyla chrysoscelis) tadpoles vary depending on whether predators are present in the pond. Tadpoles reared in ponds with predatory dragonfly larvae are relatively inactive compared with tadpoles in predator-free ponds, and have relatively large, brightly colored tailfins with dark spots along the margins. Models for the evolution of plasticity predict that induced phenotypes such as this should confer high fitness relative to the typical phenotype when in the presence of predators, but should be costly when the predator is absent. Our study tested for the predicted fitness trade-off in H. chrysoscelis by first rearing tadpoles in mesocosms under conditions that induce the alternate phenotypes, and then comparing the performance of both phenotypes in both environments. We generated the two phenotypes by rearing tadpoles in 600-liter outdoor artificial ponds that contained either two caged dragonflies (Anax junius) or an empty cage. Tadpoles from the two environments showed significantly different behavior, tail shape, and tail color within two weeks of exposure. We compared the growth and survival of both phenotypes over four weeks in ponds where there was no actual risk of predation. Under these conditions, both phenotypes grew at the same rate, but the predator-induced phenotype had significantly lower survival than the typical phenotype, indicating that induced tadpoles suffered greater mortality from causes other than odonate predation. We tested the susceptibility of both phenotypes to predation by exposing them to dragonflies in 24-h predation trials. The predator-induced phenotype showed a significant survival advantage in these trials. These results confirm that the predator-induced phenotype in H. chrysoscelis larvae is associated with fitness costs and benefits that explain why the defensive phenotype is induced rather than constitutive.     

Direct and indirect effects of dragonfly (<Emphasis Type="Italic">Anax imperator</Emphasis>) nymphs on green toad (<Emphasis Type="Italic">Bufo viridis</Emphasis>) tadpoles

We conducted an artificial pond experiment to assess the direct and indirect effects of predation on Bufo viridis tadpoles. We ran three treatments: free Anax (unrestrained predatory dragonfly nymph Anax imperator), caged Anax (non-consumptive effects), and control (no Anax). Anax showed both strong consumptive and non-consumptive effects on Bufo tadpoles. Free Anax eliminated all of the tadpoles within six days. Tadpoles preferred the shady side of the ponds. Caged Anax caused tadpoles to increase their spatial preferences. Tadpoles avoided the center of the pond, and in the presence of the caged predator, they were found in the center even less. Tadpoles also showed a strong preference for crowding together, and in the presence of a caged Anax, they tended to crowd more. Moreover, Bufo metamorphosed earlier and at a larger size in the caged Anax ponds, possibly by providing extra food resources due to the extra organic matter excreted by the predators. Handling editor: K. Martens     

The impact of larval predators and competitors on the morphology and fitness of juvenile treefrogs

Studies of phenotypic plasticity typically focus on traits in single ontogenetic stages. However, plastic responses can be induced in multiple ontogenetic stages and traits induced early in ontogeny may have lasting effects. We examined how gray treefrog larvae altered their morphology in four different larval environments and whether different larval environments affected the survival, growth, development, and morphology of juvenile frogs at metamorphosis. We then reared these juveniles in terrestrial environments under high and low intraspecific competition to determine whether the initial differences in traits at metamorphosis affected subsequent survival and growth, whether the initial phenotypic differences converged over time, and whether competition in the terrestrial environment induced further phenotypic changes. Larval and juvenile environments both affected treefrog traits. Larval predators induced relatively deep tail fins and short bodies, but there was no impact on larval development. In contrast, larval competitors induced relatively short tails and long bodies, reduced larval growth, and slowed larval development. At metamorphosis, larval predators had no effect on juvenile growth or relative morphology while larval competitors produced juveniles that were smaller and possessed relatively shorter limbs and shorter bodies. After 1 month of terrestrial competition among the juvenile frogs, the initial differences in juvenile morphology did not converge. There were no differences in growth due to larval treatment but there were differences in survival. Individuals that experienced low competition as tadpoles experienced near perfect survival as juvenile frogs but individuals that experienced high competition as tadpoles suffered an 18% decrease in survival as juvenile frogs. There were also morphological responses to juvenile competition, but these changes appear to be due, at least in part, to allometric effects. Collectively, these results demonstrate that larval environments can have profound impacts on the traits and fitness of organisms later in ontogeny.     

Predator-prey relationships among larval dragonflies,salamanders, and frogs

Summary Tadpoles of the barking tree frog, Hyla gratiosa, are abundant in spring and summer in some ponds and Carolina bays on the Savannah River Plant near Aiken, South Carolina. To determine how these tadpoles survive in the presence of predaceous salamander larvae, Ambystoma talpoideum, and larvae of an aeshnid dragonfly, Anax junius, we determined fields densities and sizes of the predators and the prey and conducted predation experiments in the laboratory. Tadpoles rapidly grow to a size not captured by Ambystoma, although Anax larvae can capture slightly larger tadpoles. Differing habitat preferences among the tadpoles and the two predator species probably aid in reducing predation pressure. Preliminary work indicates that the tadpoles may have an immobility response to an attack by a predator. In addition, the smallest, most vulnerable tadpoles have a distinctive color pattern which may function to disrupt the body outline and make them indiscernable to predators.     

Multiple predator effects on size-dependent behavior and mortality of two species of anuran larvae

This study examined the effects of multiple predators on size‐specific behavior and mortality of two species of anuran larvae. Particularly, we focused on how trait changes in predators and prey may be transmitted to other species in the food web. In laboratory experiments, we examined the effects of bluegill sunfish, Lepomis macrochirus, and the odonate larva Anax junius on behavior and mortality of tadpoles of the bullfrog, Rana catesbeiana, and the green frog R. clamitans. Experiments were conducted with predators alone and together to assess effects on behavior and mortality of the tadpoles. The experiments were replicated on five size classes of the tadpoles to evaluate how responses varied with body size.
Predation rates by Anax were higher on bullfrogs than on green frogs, and both bullfrogs and green frogs suffered greater mortality from Anax than from bluegill. Bluegill only consumed green frogs. Predation rates by both predators decreased with increasing tadpole size and decreased in the non‐lethal (caged) presence of the other predator. Both anuran larvae decreased activity when exposed to predators. Bullfrogs, however, decreased activity more in the presence of Anax than in the presence of bluegill, whereas green frogs decreased activity similarly in the presence of both predators. The largest size class of green frogs, but not of bullfrogs, exhibited spatial avoidance of bluegill. These responses were directly related to the risk posed by the different predators to each anuran species. Anax activity (speed and move frequency) also was higher when alone than in the non‐lethal presence of bluegill. We observed decreased predation rate of each predator in the non‐lethal presence of the other, apparently caused by two different mechanisms. Bluegill decreased Anax mortality on tadpoles by restricting the Anax activity. In contrast, Anax decreased bluegill mortality on tadpoles by reducing tadpole activity. We discuss how the activity and spatial responses of the tadpoles interact with palatability and body size to create different mortality patterns in the prey species and the implications of these results to direct and indirect interactions in this system.     

Increasing conspecific density weakens the ability of intermediate predators to develop induced morphological defences to top predators

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Developmental stability and genetic architecture: a comparison within and across thermal regimes in tadpoles

We investigated homogeneity of growth and development as indices of developmental stability in sibling tadpoles from two sampling regions of the common frog, Rana temporaria. One region is characterized by relatively warm breeding ponds with a short activity season (`north'), and one by relatively cool breeding ponds and a long activity season (`south'). Tadpoles from the two regions were raised in three different temperatures selected to mimic the natural variation throughout the range. The results show that (1) north tadpoles respond with a relatively greater increase in growth with increased temperature than south tadpoles, (2) mean growth rate and its coefficient of variation were negatively correlated in the temperature regime in which a population was primarily under selection in the wild, whereas no such correlation was found at temperatures more seldom encountered in the natural populations, (3) phenotypic and genetic correlations between morphological traits within individuals were positive and were relatively higher in north than south tadpoles in the warm treatment, but higher for south tadpoles in the cold treatment and (4) across thermal environments, south tadpoles showed significant genetic correlations, whereas the correlations for north tadpoles were not significantly different from zero. South tadpoles showed only positive genetic correlations (n=30), whereas 14 of 30 correlation coefficients were negative in north tadpoles. In conclusion, developmental stability for growth and morphometry was higher at `optimal' conditions and decreased at the tail ends of the reaction norms within regions, with marked differences reflecting selection history between regions.     

A growth/mortality trade-off in larval salamanders and the coexistence of intraguild predators and prey

Behavioral and morphological traits often influence a key trade-off between resource acquisition and vulnerability to predation, and understanding trait differences between species can provide critical insight into their interactions with other species and their distributions. Such an approach should enhance our understanding of the criteria for coexistence between species that can interact through both competition and predation (i.e. intraguild predators and prey). I conducted a common garden experiment that revealed strong differences between three guild members (larval salamanders Ambystoma laterale, A. maculatum, and A. tigrinum) in behavior, morphology, and growth in the presence and absence of a shared top predator (the larval dragonfly Anax longipes). All three species also reduced their activity and modified their tail fin depth, tail muscle length, and body length in response to non-lethal Anax. Species that act as intraguild predators were more active and could grow faster than their intraguild prey species, but they also suffered higher mortality in laboratory predation trials with Anax. I also used survey data from natural communities to compare the distribution of Ambystoma species between ponds differing in abiotic characteristics and predatory invertebrate assemblages. An intraguild prey species (A. maculatum) was found more reliably, occurred at higher densities, and was more likely to persist late into the larval period in ponds with more diverse invertebrate predator assemblages. Taken together, these results indicate that top predators such as Anax may play an important role in influencing intraguild interactions among Ambystoma and ultimately their local distribution patterns.     

Fish and dragonfly nymph predators induce opposite shifts in color and morphology of tadpoles

Many prey species, including amphibian larvae, can adaptively alter coloration and morphology to become more or less conspicuous to predators. Despite abundant research on predator-induced plasticity in tadpoles, the combination of color and morphological responses to predators remains largely unexplored. We measured predator-induced morphological and color plasticity in tadpoles. We reared tadpoles of the neotropical treefrog Dendropsophus ebraccatus with dragonfly nymph or fish predators, or in a predator-free control. After 10 days, we digitally photographed tadpoles and measured eight morphometric variables and five tail color variables. Tadpoles reared with nymphs developed the largest and reddest tails, but incurred a developmental cost, being the smallest overall. Cues from fish induced an opposite tail phenotype in tadpoles, causing shallow achromatic tails. Control tadpoles developed intermediate tail phenotypes. This provides the first experimental evidence that tadpoles can shift both color and morphology in opposite, predator-specific directions in response to a fish and an odonate predator. Despite mean differences, however, there was substantial variation in the degree of phenotype induction across treatments. Tail redness was correlated with tail spot size, but not perfectly, indicating that color and morphology may be partially decoupled in D. ebraccatus . Balancing selection from multiple conflicting predators may result in genetic variation for developmental plasticity.     

Specific induced responses to different predator species in anuran larvae

Models of defence against multiple enemies predict that specialized responses to each enemy should evolve only under restrictive conditions. Nevertheless, tadpoles of Rana temporaria can differentiate among several predator species. Small tadpoles used a refuge when Notonecta backswimmers were in the pond, but showed a weaker hiding response to adult Triturus alpestris newts and no response to aeshnid dragonfly larvae (Aeshna and Anax). All predators caused a decline in feeding and swimming activity. Large tadpoles reserved the strongest behavioural response for dragonflies, while Triturus caused no response. The shift during development suggests that tadpoles distinguished among predators, rather than exhibiting a graded dosage response to a single cue associated with predation. Information on habitat distributions of predators suggests that they are regularly encountered, which would facilitate evolution of adaptive behavioural responses. Morphological responses to all predators were similar, perhaps because similar morphologies defend against all four predators. The evolutionary maintenance of specialized responses to multiple predators may be possible because adaptive responses do not conflict and the predators themselves do not interact strongly.     

DELAYED COSTS OF AN INDUCED DEFENSE IN TADPOLES? MORPHOLOGY,HOPPING, AND DEVELOPMENT RATE AT METAMORPHOSIS

Models for the evolution of plasticity predict that individuals having phenotypes induced by exposure to enemies should experience relatively low fitness when enemies are absent. However, costs of induced phenotypes have been difficult to find in both plants and animals, perhaps because costs are expressed at later stages in the life cycle. We searched for delayed costs of an induced defense in larvae of the water frog Rana ridibunda, which exhibits strong phenotypic responses to predators. Tadpoles grew to metamorphosis in outdoor artificial ponds, in either the presence or absence of Aeshna dragonfly larvae confined within cages. We collected metamorphs at forelimb emergence, estimated their development rate until tail resorption was complete, and measured their body and leg shape and hopping performance. Development rate through metamorphosis reflects the duration of a transitional period during which metamorphs are especially vulnerable to predators, and hopping performance may reflect ability to escape predators. Froglets from the dragonfly treatment lost mass through metamorphosis significantly faster than those from predator-free ponds, but they resorbed their tails at about the same rate, despite the fact that their tails were relatively large to begin with. Froglets developing from predator-induced tadpoles had shorter, more muscular legs, and hopped 5% longer distances (difference not significant). Therefore, producing an induced defense against insect predators during the tadpole stage did not exact a cost during or immediately after metamorphosis; if anything, tadpoles with the predator-induced phenotype gave rise to more vigorous froglets. These results focus attention on other costs of the induced phenotype, as well as alternative explanations for plasticity that do not rely on direct fitness trade-offs.     

Risk of predation and behavioural response in three anuran species: influence of tadpole size and predator type

Many species alter their activity, microhabitat use, morphology and life history in response to predators. Predation risk is related to predator size and palatability of prey among others factors. We analyzed the predation risk of three species of tadpoles that occur in norwestern Patagonia, Argentina: Pleurodema thaul, Pleurodema bufoninum and Rhinella spinulosa. We sampled aquatic insect predators in 18 ponds to determine predator–tadpole assemblage in the study area. In laboratory conditions, we analysed the predation rate imposed by each predator on each tadpole species at different tadpole sizes. Finally, we tested whether tadpoles alter their activity in the presence of chemical and visual cues from predators. Small P. thaul and P. bufoninum tadpoles were the most vulnerable prey species, while small R. spinulosa tadpoles were only consumed by water bugs. Dragonflies and water bugs were the most dangerous tadpole predators. Small P. thaul tadpoles reduced their activity when they were exposed to all predators, while large tadpoles only reduced the activity in the presence of large predators (dragonfly larvae and water bugs). Small P. bufoninum tadpoles reduced the activity when they were exposed to beetle larvae and dragonfly larvae, while large tadpoles only reduced activity when they were exposed to larger predators (water bugs and dragonfly larvae). R. spinulosa tadpoles were the less sensitive to presence of predators, only larger tadpoles responded significantly to dragonfly larvae by reducing their activity. We conclude that behavioural responses of these anuran species were predator-specific and related to the risk imposed by each predator.     

Nonlethal injury caused by an invasive alien predator and its consequences for an anuran tadpole

Nonlethal tail injury resulting from unsuccessful predation attempts is common in anuran larvae and can potentially induce significant fitness costs in terms of survival and growth. We tested the hypotheses that the alien red swamp crayfish, Procambarus clarkii, is an important inducer of tail injury in tadpoles of the Iberian spadefoot toad, Pelobates cultripes, and that tail damage can have important consequences for the tadpoles’ life history and morphology. This was investigated by first estimating frequencies of caudal injury in P. cultripes tadpoles in temporary ponds, with and without crayfish. Secondly, we performed a laboratory experiment in which four levels of tail injury frequency were combined with two levels of food availability.The frequency of tadpoles with damaged tails was higher in ponds with crayfish and the presence of this predator was the strongest predictor of tail injury frequency in a pond. Induced tail loss decreased larval survivorship and affected tail morphology, with injured tadpoles developing deeper tail muscles and shallower tail fins. The magnitude of these effects depended on injury frequency, as well as on food availability. The results suggest that P. clarkii is inflicting tail injuries at much higher levels than those occurring before its introduction; these injuries affect tadpole morphology and may induce delayed fitness costs.