Differences In Behavioural Plasticity Research Articles

Partitioning variance in a signaling trade-off under sexual selection reveals among-individual covariance in trait allocation.

Understanding the evolution of traits subject to trade-offs is challenging because phenotypes can (co)vary at both the among- and within-individual levels. Among-individual covariation indicates consistent, possibly genetic, differences in how individuals resolve the trade-off, while within-individual covariation indicates trait plasticity. There is also the potential for consistent among-individual differences in behavioral plasticity, although this has rarely been investigated. We studied the sources of (co)variance in two characteristics of an acoustic advertisement signal that trade-off with one another and are under sexual selection in the gray treefrog, Hyla chrysoscelis: call duration and call rate. We recorded males on multiple nights calling spontaneously and in response to playbacks simulating different competition levels. Call duration, call rate, and their product, call effort, were all repeatable both within and across social contexts. Call duration and call rate covaried negatively, and the largest covariance was at the among-individual level. There was extensive plasticity in calling with changes in social competition, and we found some evidence for among-individual variance in call rate plasticity. The significant negative among-individual covariance in trait values is perpendicular to the primary direction of sexual selection in this species, indicating potential limits on the response to selection.

Individual differences in learning ability are negatively linked to behavioural plasticity in a frequency-dependent game

Behavioural plasticity can be costly, but is advantageous when it allows animals to adjust their behaviour to current conditions. Since individual differences in learning ability could be a source of differences in behavioural plasticity, the frequency dependence of payoffs within a foraging group may permit the coexistence of both plastic, fast-learning individuals and nonplastic, slow-learning individuals; in a frequency-dependent context the adjustments of a few benefit all. In this study, we investigated whether individuals that learned faster in a simple associative learning task were also more likely to adjust their behaviour in a social foraging game context than their slower-learning groupmates. We measured the associative learning ability of female Bengalese finches, Lonchura striata domestica, in a colour discrimination task and their degree of behavioural plasticity in tactic use when foraging conditions called for changes in the flock's producer–scrounger equilibrium. We found that behavioural plasticity was affected by learning speed. However, in contrast to our expectation, the slower learners were most plastic. We argue that behavioural plasticity in the producer–scrounger game context may require learning that is different from colour matching. We also propose that our results may be related to the fast–slow continuum; being proactive or fast and inaccurate could favour being responsive in simple asocial contexts while being reactive or slow and accurate could favour being plastic in more complex social contexts. Future empirical studies need to compare differences in behavioural plasticity in tactic use with learning speed measured in other types of learning tasks and with personality traits relevant to the fast–slow continuum.

Body size, but not age‐at‐maturation or context, affects the expression of predator‐induced behavioural plasticity in female green swordtails (Xiphophorus hellerii)

AbstractBehavioural plasticity is a form of reversible phenotypic plasticity in which a genotype can express different behavioural phenotypes under different environmental conditions. Though an interest in among‐individual differences in behavioural plasticity has flourished in recent decades, few studies have considered the effects of intrinsic factors, such as life‐history or morphological traits, in tandem with extrinsic factors, such as presence of conspecifics in different social contexts, on predator‐induced behavioural plasticity. Here, we present a study conducted with female green swordtail fishes, Xiphophorus hellerii, designed to assess the effects of age‐at‐maturation and body size on the expression of predator‐induced behavioural plasticity in two social contexts: (a) female‐only (two females) and (b) female‐and‐male (two females and a male). We further examined the extent to which individual expression of behavioural plasticity is consistent across these two social contexts. We found that in the presence of a predator, focal females were more timid in response to the stimulus and more tolerant of the non‐focal female, and small females expressed this change from bold/less tolerant to timid/more tolerant to a greater degree than large females, regardless of age‐at‐maturation. However, individuals were not consistent in the degree or direction of plasticity expressed in the behaviours of interest between the female‐only and the female‐and‐male context. Here, we show that within‐ and among‐individual differences in behavioural expression are common but inconsistent. How intrinsic and extrinsic factors independently or together drive expression of plasticity in antipredator and agonistic behaviours is varied and warrants further study.

Are some individuals generally more behaviorally plastic than others? An experiment with sailfin mollies.

Individuals within the same population generally differ among each other not only in their behavioral traits but also in their level of behavioral plasticity (i.e., in their propensity to modify their behavior in response to changing conditions). If the proximate factors underlying individual differences in behavioral plasticity were the same for any measure of plasticity, as commonly assumed, one would expect plasticity to be repeatable across behaviors and contexts. However, this assumption remains largely untested. Here, we conducted an experiment with sailfin mollies (Poecilia latipinna) whose behavioral plasticity was estimated both as the change in their personality traits or mating behavior across a social gradient and using their performance on a reversal-learning task. We found that the correlations between pairwise measures of plasticity were weak and non-significant, thus indicating that the most plastic individuals were not the same in all the tests. This finding might arise because either individuals adjust the magnitude of their behavioral responses depending on the benefits of plasticity, and/or individuals expressing high behavioral plasticity in one context are limited by neural and/or physiological constraints in the amount of plasticity they can express in other contexts. Because the repeatability of behavioral plasticity may have important evolutionary consequences, additional studies are needed to assess the importance of trade-offs between conflicting selection pressures on the maintenance of intra-individual variation in behavioral plasticity.

Social conformity in solitary crabs, Carcinus maenas, is driven by individual differences in behavioural plasticity

Group living is widespread in the animal kingdom and recent studies into the mechanisms underlying group cohesion and behavioural synchrony have highlighted the importance of between-individual behavioural differences (‘animal personality’). In group-living animals, social conformity occurs when animals compromise their own behaviour to the level of a certain behaviour displayed by another individual or a group, and the degree to which individuals conform can depend upon interindividual differences in behavioural types. Social conformity can increase group cohesion and ultimately predator avoidance and/or resource acquisition for group-living individuals. However, it remains unclear whether similar conformity effects exist in solitary species, many of which form temporary aggregations and, if so, whether changes in behaviour in the presence of conspecifics are dependent on individuals' personalities in solitary contexts. We studied the effects of social context (i.e. the presence of a conspecific) on behaviour in solitary shore crabs, using automated video tracking. Individuals differed consistently in their activity levels within and across contexts and were significantly more active in solitary than dyadic contexts. No differences in activity between same- and opposite-sex dyads were found. Crabs' activity levels were more similar when tested together than when tested alone, indicating a social conformity effect. Furthermore, more active behavioural types decreased their activity to a greater extent when paired with a conspecific. The sex composition of the dyad had no effect on changes in activity. Overall, our findings suggest that social conformity is moderated by individual behavioural differences in a solitary organism. It is often presumed that, over evolutionary time, the social structure of animal populations has important consequences for the evolution of personalities and vice versa. We suggest that studying solitary or facultatively social organisms may allow researchers to tease out causality between personality differences and socioecological dynamics.

Prey behavioural reaction norms: response to threat predicts susceptibility to predation

Behavioural syndromes (i.e. population-level behavioural correlations) arise when individuals, on average, maintain the same behavioural expression across different ecological contexts. Population-level syndromes can appear maladaptive, such as when prey remain active across the absence and presence of a sit-and-wait predator. Yet in nature, individuals often vary in syndrome adherence, exhibiting individual-level differences in behavioural plasticity. Here, I use an experiment to show that individual behavioural plasticity (a reduction in activity level in the presence of predation threat) increases a prey's likelihood of surviving predator exposure, and further predicts survival better than single-context activity level measures. In an additional experiment, I identify conditioning (nonlethal predator exposure) as a process that reduces prey activity level. This work demonstrates that although population-level behavioural syndromes can appear maladaptive, behavioural plasticity and conditioning could potentially ameliorate negative effects at the individual level.

Repeatability, heritability, and age-dependence of seasonal plasticity in aggressiveness in a wild passerine bird.

Labile characters allow individuals to flexibly adjust their phenotype to changes in environmental conditions. There is growing evidence that individuals can differ both in average expression and level of plasticity in this type of character. Both of these aspects are studied in conjunction within a reaction norm framework. Theoreticians have investigated the factors promoting variation in reaction norm intercepts (average phenotype) and slopes (level of plasticity) of a key labile character: behaviour. A general prediction from their work is that selection will favour the evolution of repeatable individual variation in level of plasticity only under certain ecological conditions. While factors promoting individual repeatability of plasticity have thus been identified, empirical estimates of this phenomenon are largely lacking for wild populations. We assayed aggressiveness of individual male great tits (Parus major) twice during their egg-laying stage and twice during their egg-incubation stage to quantify each male's level of seasonal plasticity. This procedure was applied during six consecutive years; all males breeding in our plots during those years were assayed, resulting in repeated measures of individual reaction norms for any individual breeding in multiple years. We quantified among- and within-individual variation in reaction norm components, allowing us to estimate repeatability of seasonal plasticity. Using social pedigree information, we further partitioned reaction norm components into their additive genetic and permanent environmental counterparts. Cross-year individual repeatability for the intercepts (average aggressiveness) and slopes (level of seasonal plasticity) of the aggressiveness reaction norms were 0·574 and 0·516 respectively. The mean of the posterior distributions suggested modest heritabilities (h2 =0·260 for intercepts; h2 =0·266 for slopes), but these estimates were relatively uncertain. Males behaved more aggressively in areas with higher breeding densities, and became less aggressive and less plastic with increasing age; plasticity thus varied within individuals and was multidimensional in nature. This empirical study quantified cross-year individual repeatability, heritability and age-related reversible plasticity in behaviour. Acknowledging such patterns of multi-level variation is important not only for testing behavioural ecology theory concerning the evolution of repeatable differences in behavioural plasticity but also for predicting how reversible plasticity may evolve in natural populations.

Personality, plasticity, and resource defense

In many animal taxa, behavior varies both among individuals (animal “personalities”) and within individuals (“plasticity”). Personality and plasticity may co-vary if individuals differ in responsiveness to changes in their environment (“I × E” interaction). The nature and fitness implications of individual differences in behavioral plasticity in the wild are poorly understood. In territorial animals, fitness depends fundamentally on resource-defense behavior—their response to various threats from conspecific competitors. Such systems thus offer an ideal opportunity to investigate individual differences in behavioral plasticity. We used male superb fairy-wrens (Malurus cyaneus) to test for individual differences in the intensity and plasticity of territorial defense behavior. Using captive assays, we identified behavioral types on the basis of fast versus slow exploration of a novel environment (the “proactive–reactive” axis of behavior). Then we simulated territorial intrusions in the wild, using playback of experimentally manipulated songs that differed in trill length in a pair-wise design. Although previous work suggests that proactive individuals are more aggressive and less responsive than reactive individuals, we found no support for these differences in the context of territorial defense in the wild. Fast explorers (proactive) and slow explorers (reactive) responded equally aggressively to a simulated territorial intrusion overall. Furthermore, although fast explorers responded equally strongly to the two different playback stimuli, there was little evidence that slow explorers differentiated between the two stimuli, and this “I × E” interaction was not statistically significant. Further work is needed to determine the prevalence in the wild of personality-related differences in behavioral plasticity.

Behavioural responses in a net restraint test predict interrenal reactivity in Arctic charr Salvelinus alpinus.

In this study, a 1 min net restraint test was evaluated as a method to predict stress-coping style in Arctic charr Salvelinus alpinus, by investigating the relationship between behaviour during the test and levels of plasma cortisol sampled after 30 min confinement. In two separate groups of S. alpinus, general linearized model revealed significant correlations between cortisol levels and principal component scores extracted from principal component analysis, combining measures of activity in the tests. With the use of glmulti, the model selection ruled out any effects of size, sex and order of capture on interrenal reactivity. In general, S. alpinus that were more active in the net restraint test also had low levels of circulating cortisol, suggesting a proactive coping style. The results from two repeated runs were not correlated, but both runs, performed eight days apart, show a negative correlation between post-stress cortisol level and activity in the net. The lack of consistency could be explained by different treatments before each run and individual differences in behavioural plasticity. The net restraint test is thus predictive of stress-coping style in S. alpinus, and has the benefit of being less time-consuming than the commonly used confinement stress test.

Evolution of individual variation in behaviour and behavioural plasticity under scramble competition

In scramble competition mating systems, individual behaviours related to male–male competition are expected to be plastic across sociosexual environments. However, the evolutionary forces that shape individual differences in behavioural plasticity remain poorly understood. We measured behaviour associated with scramble competition in male water striders, Tenagogerris euphrosyne, in two social contexts. Male T. euphrosyne tend to mount other individuals or pairs indiscriminately and then dismount if their target is either another male or a mating pair. We measured the speed with which a focal male dismounted (i.e. his sensitivity to having made an inappropriate mounting) in each of these contexts. We quantified temporal consistency of dismount speed within each context, as well as individual variation in behavioural plasticity across contexts. We then estimated the effect of the behaviour and of plasticity on individual fitness in different sex ratio conditions. We found that individuals differed in their recognition sensitivity traits, and also in how plastic their sensitivity (i.e. dismount speed) was to context (mating status or sex). When we measured the mating success of each male within experimental groups kept at four different sex ratios, recognition sensitivity traits in both contexts interacted to influence mating success, and there were significant differences in linear selection on sensitivity traits between sex ratio treatments. We discuss how insensitive males evolve, and how individual variation in behavioural plasticity could be maintained by selection or environmental variability.

Between-individual differences in behavioural plasticity within populations: causes and consequences

Behavioural traits are characterized by their labile expression: behavioural responses can, in principle, be up- and down-regulated in response to moment-to-moment changes in environmental conditions. Evidence is accumulating that individuals from the same population differ in the degree and extent of this form of phenotypic plasticity. We here discuss how such between-individual differences in behavioural plasticity can result from additive and interactive effects of genetic make-up and past environmental conditions, and under which conditions natural selection might favour this form of between-individual variation. We highlight how spatial or temporal variation in the environment, in combination with competition among individuals, can promote adaptive individual differences in plasticity; and we detail how differences in plasticity can emerge as a result of selection pressures induced by social interactions or as a response to between-individual differences in state. We further discuss both ecological and evolutionary consequences of individual differences in plasticity. We outline, for example, how individual differences in plasticity can have knock-on effects on the rate of evolution; and how such differences can enhance the stability and persistence of populations.

Personality and plasticity: consistent responses within-, but not across-temperature situations in crabs

Recent research suggests that repeated assays of behaviour, conducted both within and across situations, could reveal important insights into two traditionally distinct areas of study: animal personality and individual differences in behavioural plasticity. However, at present relatively few studies present such data, and few consider how changing abiotic conditions affect behavioural plasticity. Individual differences in metabolic rate have been suggested as a proximate mechanism promoting personality, leading one to speculate that individual differences in metabolic sensitivity to temperature may affect behavioural responses in ectotherms. At present, only one study (out of two) has tested for and shown individual differences in behavioural responses to temperature. Here, we repeatedly assayed the behaviour of a marine crab across a narrow range of temperatures to test for individual differences in responses to temperature. We observed large inter-individual differences in behaviour that were consistent over time at a given temperature (evidence for personality), and individual differences in responses to temperature (evidence for plasticity). This study adds to the very scant literature on ectotherm behavioural sensitivity to temperature, and suggests the phenomenon might be widespread. We speculate about the role of metabolism as a proximate mechanism that might explain these individual differences in plasticity and make suggestions for future research to test this hypothesis.

Adaptive strategies for managing uncertainty may explain personality‐related differences in behavioural plasticity

There is growing evidence that individuals within populations show consistent differences in their behaviour across contexts (personality), and that personality is associated with the extent to which individuals adjust their behaviour as function of changing conditions (behavioural plasticity). We propose an evolutionary explanation for a link between personality and plasticity based upon how individuals manage uncertainty. Individuals can employ three categories of tactics to manage uncertainty. They can 1) gather information (sample) to reduce uncertainty, 2) show strategic (state‐dependent) preferences for options that differ in their associated variances in rewards (i.e. variance‐sensitivity), or 3) invest in insurance to mitigate the consequences of uncertainty. We explicitly outline how individual differences in the use of any of these tactics can generate personality‐related differences in behavioural plasticity. For example, sampling effort is likely to co‐vary with individual activity and exploration behaviours, while simultaneously creating population variation in reactions to changes in environmental conditions. Individual differences in the use of insurance may be associated with differences in risk‐taking behaviours, such as boldness in the face of predation, thereby influencing the degree of adaptive plasticity across individuals. Population variation in responsiveness to environmental changes may also reflect individual differences in variance‐sensitivity, because stochastic change in the environment increases variances in rewards, which may both attract and benefit variance‐prone individuals, but not variance‐averse individuals. We review the existing evidence that individual variation in strategies for managing uncertainty exist, and describe how positive‐feedbacks between sampling, variance‐sensitivity and insurance can maintain and exaggerate even small initial differences between individuals in the relative use of these tactics. Given the pervasiveness of the problem of uncertainty, alternative strategies for managing uncertainty may provide a powerful explanation for consistent differences in behaviour and behavioural plasticity for a wide range of traits.

Disentangling the roles of frequency-vs. state-dependence in generating individual differences in behavioural plasticity

Theoretical work suggests that both negative frequency-dependent payoffs and state-dependent payoffs can lead to individual variation in behavioural plasticity. We investigated the roles of both frequency- and state-dependence on the occurrence of individual variation in behavioural plasticity in a series of experiments where we manipulated perceived predation danger for red knots (Calidris canutus islandica). We found individual variation in plasticity in a trait with negative frequency-dependent payoffs (vigilance), but not in a trait with positive frequency-dependent payoffs (escape flights). Furthermore, there was no correlation between the average level of vigilance under low predation danger and the magnitude of response to increased predation danger, as would be expected under state-dependence. Thus, our results provide support for the hypothesis that negative-frequency dependence favours individual variation in plasticity. However, negative-frequency dependence alone cannot explain why plasticity would be consistent within individuals, and future studies should address the factors that might favour individual consistency.

Variation in personality and behavioural plasticity across four populations of the great tit Parus major

1. Interest in the evolutionary origin and maintenance of individual behavioural variation and behavioural plasticity has increased in recent years. 2. Consistent individual behavioural differences imply limited behavioural plasticity, but the proximate causes and wider consequences of this potential constraint remain poorly understood. To date, few attempts have been made to explore whether individual variation in behavioural plasticity exists, either within or between populations. 3. We assayed 'exploration behaviour' among wild-caught individual great tits Parus major when exposed to a novel environment room in four populations across Europe. We quantified levels of individual variation within and between populations in average behaviour, and in behavioural plasticity with respect to (i) repeated exposure to the room (test sequence), (ii) the time of year in which the assays were conducted and (iii) the interval between successive tests, all of which indicate habituation to novelty and are therefore of functional significance. 4. Consistent individual differences ('I') in behaviour were present in all populations; repeatability (range: 0.34-0.42) did not vary between populations. Exploration behaviour was also plastic, increasing with test sequence - but less so when the interval between subsequent tests was relatively large - and time of year; populations differed in the magnitude of plasticity with respect to time of year and test interval. Finally, the between-individual variance in exploration behaviour increased significantly from first to repeat tests in all populations. Individuals with high initial scores showed greater increases in exploration score than individuals with low initial scores; individual by environment interaction ('I × E') with respect to test sequence did not vary between populations. 5. Our findings imply that individual variation in both average level of behaviour and behavioural plasticity may generally characterize wild great tit populations and may largely be shaped by mechanisms acting within populations. Experimental approaches are now needed to confirm that individual differences in behavioural plasticity (habituation) - not other hidden biological factors - caused the observed patterns of I × E. Establishing the evolutionary causes and consequences of this variation in habituation to novelty constitutes an exciting future challenge.

Plasticity in reproductive behaviour in two populations of the peacock blenny

Summary In the peacock blenny (Salaria pavo) the reproductive behaviour is described to vary between two populations that differ in nest availability. At the Gulf of Trieste (GT), Italy, where nest availability is high, conventional sex roles are present and males adopting an alternative parasitic reproductive tactic are rare. Conversely, at Ria Formosa (RF), Portugal, where nest site availability is low, females are the courting sex and a high percentage of parasitic males occur. Laboratory experiments were used to study the degree of plasticity of the reproductive behaviours used by females and by the two male morphs in both populations. Nesting males were sequentially presented with a female and a female-like parasitic male and the reproductive behaviours of all fish were quantified. Under similar laboratory conditions, nesting males from both populations did not differ in sexual or agonistic displays towards females or parasitic males, showing that males from the sex-reversed population are also able to express significant levels of courtship. In contrast, females followed the typical population pattern, with females from RF courting nesting males more and more readily than females from GT. We hypothesised that apparent differences in behavioural plasticity between nesting males and females were a consequence of the perception of the presence of eggs in the nest. Nesting males from both populations received an empty nest during test trials and, thus, had to court females in order to receive a first spawn. On the other hand, females were probably unaware of the presence or absence of eggs when presented to the nesting male and assumed the population typical courtship profile. Interestingly, the parasitic males’ behaviour towards

Individual differences in plasticity and sampling when playing behavioural games

When engaged in behavioural games, animals can adjust their use of alternative tactics until groups reach stable equilibria. Recent theory on behavioural plasticity in games predicts that individuals should differ in their plasticity or responsiveness and hence in their degree of behavioural adjustment. Moreover, individuals are predicted to be consistent in their plasticity within and across biological contexts. These predictions have yet to be tested empirically and so we examine the behavioural adjustment of individual nutmeg mannikins (Lonchura punctulata), gregarious ground-feeding passerines, when playing two different social foraging games: producer-scrounger (PS) and patch-choice (PC) games. We found: (i) significant individual differences in plasticity and sampling behaviour in each of the two games, (ii) individual differences in sampling behaviour were consistent over different test conditions within a game (PC) and over a six month period (PS), (iii) but neither individual plasticity nor sampling behaviour was correlated from one social foraging game to another. The rate at which birds sampled alternative tactics was positively associated with seed intake in PS trials but negatively associated in PC trials. These results suggest that games with frequency dependence of pay-offs can maintain differences in behavioural plasticity but that an important component of this plasticity is group- and/or context-specific.

Habituation to low-risk predators improves body condition in lizards

Habituation to nonlethal predation stimuli may provide benefits for animals living in areas with frequent encounters with low-risk predators. On the other hand, individuals can be very consistent in their antipredator responses, with shy individuals showing greater degree of responsiveness than bold individuals. However, the link between habituation or boldness and individual benefits has not been thoroughly investigated. We established whether and how two behavioral components associated with antipredator responses (habituation and boldness, and their interaction) would influence body condition, which is a parameter related to fitness. We conducted an outdoor semi-natural experiment with Iberian wall lizards (Podarcis hispanica). Individual boldness was consistent across contexts, but we did not find any effect of boldness or the interaction between boldness and habituation on body condition. However, those individuals that habituated more readily to a frequent predatory stimulus were able to increase their body condition more relative to lizards that habituated less. This finding highlights the importance of individual differences in behavioral plasticity, which could influence traits related to fitness. Habituation can provide benefits for individuals exposed to low-risk predators; however, individuals more prone to habituation could also experience mortality costs by wrongly habituating to a dangerous predator.

Androgens enhance plasticity of an electric communication signal in female knifefish, Brachyhypopomus pinnicaudatus

Sex steroids were initially defined by their actions shaping sexually dimorphic behavioral patterns. More recently scientists have begun exploring the role of steroids in determining sex differences in behavioral plasticity. We investigated the role of androgens in potentiating circadian, pharmacological, and socially-induced plasticity in the amplitude and duration of electric organ discharges (EODs) of female gymnotiform fish. We first challenged female fish with injections of serotonin (5-HT) and adrenocorticotropic hormone (ACTH), and with social encounters with female and male conspecifics to characterize females' pre-implant responses to each treatment. Each individual was then implanted with a pellet containing dihydrotestosterone (DHT) concentrations of 0.0, 0.03, 0.1, 0.3, or 1.0 mg 10 g − 1 body weight. We then repeated all challenges and compared each female's pre- and post-implant responses. The highest implant dose enhanced EOD duration modulations in response to all challenge types, responses to male challenge were also greater at the second highest dose, and responses to ACTH challenge were enhanced in females receiving all but the smallest dose (and blank) implants. Alternatively, amplitude modulations were enhanced only during female challenges and only when females received the highest DHT dose. Our results highlight the differential regulation of EOD duration and amplitude, and suggest that DHT enhanced the intrinsic plasticity of the electrogenic cells that produce the EOD rather than modifying behavioral phenotypes. The relative failure of DHT to enhance EOD amplitude plasticity also implies that factors other than androgens are involved in regulating/promoting male-typical EOD circadian rhythms and waveform modulations displayed in social contexts.