Predator-induced morphological plasticity across local populations of a freshwater snail

The expression of anti-predator adaptations may vary on a spatial scale, favouring traits that are advantageous in a given predation regime. Besides, evolution of different developmental strategies depends to a large extent on the grain of the environment and may result in locally canalized adaptations or, alternatively, the evolution of phenotypic plasticity as different predation regimes may vary across habitats. We investigated the potential for predator-driven variability in shell morphology in a freshwater snail, Radix balthica, and whether found differences were a specialized ecotype adaptation or a result of phenotypic plasticity. Shell shape was quantified in snails from geographically separated pond populations with and without molluscivorous fish. Subsequently, in a common garden experiment we investigated reaction norms of snails from populations' with/without fish when exposed to chemical cues from tench (Tinca tinca), a molluscivorous fish. We found that snails from fish-free ponds had a narrow shell with a well developed spire, whereas snails that coexisted with fish had more rotund shells with a low spire, a shell morphology known to increase survival rate from shell-crushing predators. The common garden experiment mirrored the results from the field survey and showed that snails had similar reaction norms in response to chemical predator cues, i.e. the expression of shell shape was independent of population origin. Finally, we found significant differences for the trait means among populations, within each pond category (fish/fish free), suggesting a genetic component in the determination of shell morphology that has evolved independently across ponds.     

Shaped by the past,acting in the present: transgenerational plasticity of anti‐predatory traits

Phenotypic expression can be altered by direct perception of environmental cues (within‐generation phenotypic plasticity) and by the environmental cues experienced by previous generations (transgenerational plasticity). Few studies, however, have investigated how the characteristics of phenotypic traits affect their propensity to exhibit plasticity within and across generations. We tested whether plasticity differed within and across generations between morphological and behavioral anti‐predator traits of Physa acuta, a freshwater snail. We reared 18 maternal lineages of P. acuta snails over two generations using a full factorial design of exposure to predator or control cues and quantified adult F₂ shell size, shape, crush resistance, and anti‐predator behavior – all traits which potentially affect their ability to avoid or survive predation attempts. We found that most morphological traits exhibited transgenerational plasticity, with parental exposure to predator cues resulting in larger and more crush‐resistant offspring, but shell shape demonstrated within‐generation plasticity. In contrast, we found that anti‐predator behavior expressed only within‐generation plasticity such that offspring reared in predator cues responded less to the threat of predation than control offspring. We discuss the consequences of this variation in plasticity for trait evolution and ecological dynamics. Overall, our study suggests that further empirical and theoretical investigation is needed in what types of traits are more likely to be affected by within‐generational and transgenerational plasticity.     

Environmental calcium modifies induced defences in snails

Inducible defences are adaptive phenotypes that arise in response to predation threats. Such plasticity incurs costs to individuals, but there has been little interest in how such induced traits in animals may be constrained by environmental factors. Here, we demonstrate that calcium availability interacts with predation cues to modify snail shell growth and form. Small snails increased their growth and were heavier when exposed to fish chemical cues, but this response was calcium limited. There was also an interactive effect of fish cues and calcium on the shell growth of larger snails, but shell strength and aperture narrowness were affected by calcium alone. For small snails, behavioural avoidance was greatest for snails exhibiting least morphological plasticity, suggesting a trade-off. There was no trade-off of somatic growth with plasticity. We suggest that the expression of defensive traits in molluscs can be constrained by calcium availability, which has implications for molluscan ecology and evolution.     

Life-history plasticity and inbreeding depression under mate limitation and predation risk: cumulative lifetime fitness dissected with a life table response experiment

Environmental effects on the evolution of mating systems are increasingly discussed, but we lack many examples of how environmental conditions affect the expression and consequences of alternative mating systems. Variation in mate availability sets up a trade-off between reproductive assurance and inbreeding depression, but the consequences of both mate limitation and inbreeding may depend on other environmental conditions. Predation risk is common under natural conditions, and known to affect allocation to reproduction, but we know little about the effects of isolation and inbreeding under predation risk. We reared selfed and outcrossed hermaphroditic freshwater snails (Physa acuta) in four environments (predator cues present or absent crossed with mating partners available or not) and quantified life-history traits and cumulative lifetime fitness. Our results confirm that isolation from mates can increase longevity and growth, resulting in higher lifetime fecundity. Thus, we observed no evidence for mate limitation of reproduction. However, reproduction under isolation (i.e., selfing) resulted in inbreeding depression, which should counteract the benefits of selfing. Inbreeding depression in fitness occurred in both predator and no-predator environments, but there was no overall change in inbreeding depression with predator cues. This represents, to our knowledge, the first empirical estimate of the effect of predation risk on inbreeding depression in an animal. Cumulative fitness was most influenced by early survival and especially early fecundity. As predation risk and inbreeding (both ancestral and due to a lack of mates) reduced early fecundity, these effect are predicted to have important contributions to population growth under natural conditions. Therefore life-history plasticity (e.g., delayed reproduction) is likely to be very important to overall fitness.     

Predator regime influences innate anti-predator behaviour in the freshwater gastropod Lymnaea stagnalis

1. Predation incurs high fitness costs in aquatic organisms either through direct consumption or through avoidance responses that reduce time for activities such as feeding and reproduction. Hence, avoidance responses of aquatic organisms should vary to match closely the predation threat in their environment.
2. The freshwater gastropod Lymnaea stagnalis occurs in a variety of environments which vary in the presence or absence of predatory fish. We used naïve snails reared from six populations of this species experiencing different predator regimes (three co-occurring with molluscivorous fish and three without) to assess whether populations differed in the type and degree of their avoidance behaviours. Innate behavioural responses to four treatments (control, conspecific alarm cues, fish kairomones and fish kairomones paired with alarm cue) were compared in laboratory trials.
3. The primary anti-predator behaviour of L. stagnalis in response to fish kairomones was to crawl out of the water rather than seek refuge under water. This response was strongest when fish kairomones were paired with alarm cues, and varied depending on population origin; snails reared from populations co-occurring with predatory fish showed a stronger response than those raised from populations not experiencing such predators. In addition, populations co-occurring with predatory fish responded to the fish kairomones presented alone.
4. Our findings suggest that the degree of innate anti-predator behaviour shown by L. stagnalis , in terms of both the level of risk to which it responds and the degree of response, varies depending on the predator regime experienced by field populations. Together with previous work on cue association, this demonstrates that this gastropod is able to match its avoidance behaviour very closely to short and long term predation threats within its habitat.     

LOCAL ADAPTATION AND THE EVOLUTION OF PHENOTYPIC PLASTICITY IN TRINIDADIAN GUPPIES (POECILIA RETICULATA)

Divergent selection pressures across environments can result in phenotypic differentiation that is due to local adaptation, phenotypic plasticity, or both. Trinidadian guppies exhibit local adaptation to the presence or absence of predators, but the degree to which predator‐induced plasticity contributes to population differentiation is less clear. We conducted common garden experiments on guppies obtained from two drainages containing populations adapted to high‐ and low‐predation environments. We reared full‐siblings from all populations in treatments simulating the presumed ancestral (predator cues present) and derived (predator cues absent) conditions and measured water column use, head morphology, and size at maturity. When reared in presence of predator cues, all populations had phenotypes that were typical of a high‐predation ecotype. However, when reared in the absence of predator cues, guppies from high‐ and low‐predation regimes differed in head morphology and size at maturity; the qualitative nature of these differences corresponded to those that characterize adaptive phenotypes in high‐ versus low‐predation environments. Thus, divergence in plasticity is due to phenotypic differences between high‐ and low‐predation populations when reared in the absence of predator cues. These results suggest that plasticity might initially play an important role during colonization of novel environments, and then evolve as a by‐product of adaptation to the derived environment.     

Cue reliability, risk sensitivity and inducible morphological defense in a marine snail

Reliable cues that communicate current or future environmental conditions are a requirement for the evolution of adaptive phenotypic plasticity, yet we often do not know which cues are responsible for the induction of particular plastic phenotypes. I examined the single and combined effects of cues from damaged prey and predator cues on the induction of plastic shell defenses and somatic growth in the marine snail Nucella lamellosa. Snails were exposed to chemical risk cues from a factorial combination of damaged prey presented in isolation or consumed by predatory crabs (Cancer productus). Water-borne cues from damaged conspecific and heterospecific snails did not affect plastic shell defenses (shell mass, shell thickness and apertural teeth) or somatic growth in N. lamellosa. Cues released by feeding crabs, independent of prey cue, had significant effects on shell mass and somatic growth, but only crabs consuming conspecific snails induced the full suite of plastic shell defenses in N. lamellosa and induced the greatest response in all shell traits and somatic growth. Thus the relationship between risk cue and inducible morphological defense is dependent on which cues and which morphological traits are examined. Results indicate that cues from damaged conspecifics alone do not trigger a response, but, in combination with predator cues, act to signal predation risk and trigger inducible defenses in this species. This ability to “label” predators as dangerous may decrease predator avoidance costs and highlights the importance of the feeding habits of predators on the expression of inducible defenses.     

Energetic costs, underlying resource allocation patterns, and adaptive value of predator-induced life-history shifts

We studied costs and benefits of life history shifts of water fleas (genus Daphnia ) in response to infochemicals from planktivorous fish. We applied a dynamic energy budget model to investigate the resource allocation patterns underlying the observed life history shifts and their adaptive value under size selective predation in one coherent analysis. Using a published data set of life history shifts in response to fish infochemicals we show that Daphnia invests less energy in somatic growth in the fish treatment. This observation complies with theoretical predictions on optimal resource allocation. However, the observed patterns of phenotypic plasticity cannot be explained by changes in resource allocation patterns alone because our model-based analysis of the empirical data clearly identified additional bioenergetic costs in the fish treatments. Consequently, the response to fish kairomone only becomes adaptive if the intensity of size selective predation surpasses a certain critical level. We believe that this is the first study that puts resource allocation, energetic costs, and adaptive value of predator induced life-history shifts – using empirical data – into one theoretical framework.     

Putting prey back together again: integrating predator-induced behavior,morphology, and life history

The last decade has seen an explosion in the number of studies exploring predator-induced plasticity. Recently, there has been a call for more comprehensive approaches that can identify functional relationships between traits, constraints on phenotypic responses, and the cost and benefits of alternative phenotypes. In this study, we exposed Helisoma trivolvis, a freshwater snail, to a factorial combination of three resource levels and five predator environments (no predator, one or two water bugs, and one or two crayfish) and examined ten traits including behavior, morphology, and life history. Each predator induced a unique suite of behavioral and morphological responses. Snails increased near-surface habitat use with crayfish but not with water bugs. Further, crayfish induced narrow and high shells whereas water bugs induced wide shells and wide apertures. In terms of life history, both predators induced delayed reproduction and greater mass at reproduction. However, crayfish induced a greater delay in reproduction that resulted in reduced fecundity whereas water bugs did not induce differences in fecundity. Resource levels impacted the morphology of H. trivolvis; snails reared with greater resource levels produced higher shells, narrower shells, and wider apertures. Resource levels also impacted snail life history; lower resources caused longer times to reproduction and reduced fecundity. Based on an analysis of phenotypic correlations, the morphological responses to each predator most likely represent phenotypic trade-offs. Snails could either produce invasion-resistant shells for defense against water bugs or crush-resistant shells for defense against crayfish, but not both. Our use of a comprehensive approach to examine the responses of H. trivolvis has provided important information regarding the complexity of phenotypic responses to different environments, the patterns of phenotypic integration across environments, and the potential costs and benefits associated with plastic traits.     

Effects of perceived predation risk and social environment on the development of three‐spined stickleback (Gasterosteus aculeatus) morphology

Phenotypically plastic changes in response to variation in perceived predation risk are widespread, but little is known about if and how social environment modulates induced responses to predation risk. We investigated the influence of perceived predation risk (i.e. chemical cues from a predator) and social environment (i.e. one, two or 20 individuals reared together) on three‐spined stickleback (Gasterosteus aculeatus) morphology in a factorial common garden experiment. We found that exposure to chemical cues from potential predators did not influence growth or body condition or induce more robust morphological defences (i.e. lateral plate numbers and dorsal spine lengths). However, sticklebacks exposed to predator cues developed longer caudal peduncles and larger eyes as compared with fish from the control treatment. As these responses may improve sticklebacks’ ability to avoid piscine predation, they might be adaptive. Social environment/density also influenced expression of some traits, but these effects were independent of predation‐risk treatment effects. In general, these results suggest that apart from the classic morphological defence structures, which appear mostly constitutive, three‐spined sticklebacks are capable of expressing potentially adaptive morphological responses to chemical cues from potential predators.     

Local adaptation and embryonic plasticity affect antipredator traits in hatchling pond snails

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Inbreeding and adaptive plasticity: an experimental analysis on predator‐induced responses in the water flea Daphnia

Several studies have emphasized that inbreeding depression (ID) is enhanced under stressful conditions. Additionally, one might imagine a loss of adaptively plastic responses which may further contribute to a reduction in fitness under environmental stress. Here, we quantified ID in inbred families of the cyclical parthenogen Daphnia magna in the absence and presence of fish predation risk. We test whether predator stress affects the degree of ID and if inbred families have a reduced capacity to respond to predator stress by adaptive phenotypic plasticity. We obtained two inbred families through clonal selfing within clones isolated from a fish pond. After mild purging under standardized conditions, we compared life history traits and adaptive plasticity between inbred and outbred lineages (directly hatched from the natural dormant egg bank of the same pond). Initial purging of lineages under standardized conditions differed among inbred families and exceeded that in outbreds. The least purged inbred family exhibited strong ID for most life history traits. Predator‐induced stress hardly affected the severity of ID, but the degree to which the capacity for adaptive phenotypic plasticity was retained varied strongly among the inbred families. The least purged family overall lacked the capacity for adaptive phenotypic plasticity, whereas the family that suffered only mild purging exhibited a potential for adaptive plasticity that was comparable to the outbred population. We thus found that inbred offspring may retain the capacity to respond to the presence of fish by adaptive phenotypic plasticity, but this strongly depends on the parental clone engaging in selfing.     

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.     

Costly plastic morphological responses to predator specific odour cues in three-spined sticklebacks (<Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis>)

Predation risk is one of the major forces affecting phenotypic variation among and within animal populations. While fixed anti-predator morphologies are favoured when predation level is consistently high, plastic morphological responses are advantageous when predation risk is changing temporarily, spatially, or qualitatively. Three-spined sticklebacks (Gasterosteus aculeatus) are well known for their substantial variability in morphology, including defensive traits. Part of this variation might be due to phenotypic plasticity. However, little is known about sticklebacks’ plastic ability to react morphologically to changing risks of predation and about the proximate cues involved. Using a split-clutch design we show that odour of a predatory fish induces morphological changes in sticklebacks. Under predation risk, i.e., when exposed to odour of a predator, fish grew faster and developed a different morphology, compared to fish reared under low predation risk, i.e., exposed to odour of a non-predatory fish, or in a fish-free environment. However, fast growing comes at cost of increased body asymmetries suggesting developmental constraints. The results indicate that sticklebacks are able to distinguish between predatory and non-predatory fishes by olfactory cues alone. As fishes were fed on invertebrates, this reaction was not induced by chemical cues of digested conspecifics, but rather by predator cues themselves. Further, the results show that variation in body morphology in sticklebacks has not only a strong genetical component, but is also based on plastic responses to different environments, in our case different predation pressures, thus opening new questions for this model species in ecology and evolution.     

Camouflaged or tanned: plasticity in freshwater snail pigmentation

By having phenotypically plastic traits, many organisms optimize their fitness in response to fluctuating threats. Freshwater snails with translucent shells, e.g. snails from the Radix genus, differ considerably in their mantle pigmentation patterns, with snails from the same water body ranging from being completely dark pigmented to having only a few dark patterns. These pigmentation differences have previously been suggested to be genetically fixed, but we propose that this polymorphism is owing to phenotypic plasticity in response to a fluctuating environment. Hence, we here aimed to assess whether common stressors, including ultraviolet radiation (UVR) and predation, induce a plastic response in mantle pigmentation patterns of Radix balthica. We show, in contrast to previous studies, that snails are plastic in their expression of mantle pigmentation in response to changes in UVR and predator threats, i.e. differences among populations are not genetically fixed. When exposed to cues from visually hunting fish, R. balthica increased the proportion of their dark pigmentation, suggesting a crypsis strategy. Snails increased their pigmentation even further in response to UVR, but this also led to a reduction in pattern complexity. Furthermore, when exposed to UVR and fish simultaneously, snails responded in the same way as in the UVR treatment, suggesting a trade-off between photoprotection and crypsis.     

Rapid evolution in response to introduced predators II: the contribution of adaptive plasticity

Background  

Introductions of non-native species can significantly alter the selective environment for populations of native species, which can respond through phenotypic plasticity or genetic adaptation. We examined phenotypic and genetic responses of Daphnia populations to recent introductions of non-native fish to assess the relative roles of phenotypic plasticity versus genetic change in causing the observed patterns. The Daphnia community in alpine lakes throughout the Sierra Nevada of California (USA) is ideally suited for investigation of rapid adaptive evolution because there are multiple lakes with and without introduced fish predators. We conducted common-garden experiments involving presence or absence of chemical cues produced by fish and measured morphological and life-history traits in Daphnia melanica populations collected from lakes with contrasting fish stocking histories. The experiment allowed us to assess the degree of population differentiation due to fish predation and examine the contribution of adaptive plasticity in the response to predator introduction.     

Divergent phenotypic responses to predators and cyanobacteria in Daphnia lumholtzi

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Temporal environmental variation and phenotypic plasticity: a mechanism underlying priority effects

Understanding the role of history in the formation of communities has been a major challenge in community ecology. Here, we explore the role of phenotypic plasticity and its associated trait‐mediated indirect interactions as a mechanism behind priority effects. Using organisms with inducible defenses as a model system, we examine how aquatic communities initially containing different predator environments are affected at the individual and community level by the colonization of a second predator. Snails and tadpoles were established in four different caged‐predator environments (no predator, fish, crayfish or water bugs). These four communities were then crossed with three predator colonization treatments (no colonization, early colonization, or late colonization) using lethal water bugs as the predator. The snails responded to the caged predator environments with predator‐specific behavioral and morphological defenses. In the colonization treatments, snails possessing the wrong phenotype attempted to induce phenotypic changes to defend themselves against the new risk. However, snails initially induced by a different predator environment often suffered high predation rates. Hence, temporal variation in predation risk not only challenged the snail prey to try to track this environmental variation through time by adjusting their defensive phenotypes, but also caused trait‐mediated interactions between snails and the colonizing predator. For tadpoles within these communities, there was little evidence that the morphological responses of snails indirectly effected tadpole predation rates by colonizing water bugs. Unexpectedly, predation rates on tadpoles by colonizing water bugs were generally higher in the three caged‐predator treatments, suggesting that water bugs elevated their foraging activity in response to potentially competing predators. In summary, we demonstrate an important priority effect in which the initial occurrence of one species of predator can facilitate predation by a second predator that colonizes at a later date (i.e. a TMII) suggesting that phenotypic plasticity can be an important driver behind priority effects (i.e. historical exposure to predators).     

Rapid evolution and behavioral plasticity following introduction to an environment with reduced predation risk

Adaptive behavioral plasticity can play a beneficial role when a population becomes established in a novel environment if environmental cues allow the expression of appropriate behavior. Further, plasticity itself can evolve over time in a new environment causing changes in the way or degree to which animals respond to environmental cues. Colonization events provide an opportunity to investigate such relationships between behavioral plasticity and adaptation to new environments. Here, we investigated the evolution of behavior and behavioral plasticity during colonization of a new environment, by testing if female mate‐choice behavior diverged in Trinidadian guppies 2–3 years (~6–9 generations) after being introduced to four locations with reduced predation risk. We collected wild‐caught fish from the source and introduced populations, and we reared out second‐generation females in the laboratory with and without predator cues to examine their plastic responses to a bright and dull male. We found introduced females were less responsive to males when reared without predator cues, but both introduced and source females were similarly responsive when reared with predator cues. Thus, the parallel evolution of behavior across multiple populations in the low‐predation environment was only observed in the treatment mimicking the introduction environment. Such results are consistent with theory predicting that the evolution of plasticity is a by‐product of differential selection across environments.