Experience during development triggers between‐individual variation in behavioural plasticity

Abstract

Behavioural consistency within and across behaviours (animal personality and behavioural syndrome, respectively) has been vigorously studied in the last decade, leading to the emergence of "animal personality" research. It has been proposed recently that not only mean behaviour (behavioural type), but the environmentally induced behavioural change (behavioural plasticity) might also differ between individuals within populations. While case studies presenting between-individual variation in behavioural plasticity have started to accumulate, the mechanisms behind its emergence are virtually unknown. We have recently demonstrated that ecologically relevant environmental stimuli during ontogeny are necessary for the development of animal personality and behavioural syndromes. However, it is unknown whether between-individual variation in behavioural plasticity is hard-wired or induced. Here, we tested whether experience with predation during development affected predator-induced behavioural plasticity in Rana dalmatina tadpoles. We ran a common garden experiment with two ontogenetic predation treatments: tadpoles developed from hatching in either the presence or absence of olfactory predator stimuli. Then, we assayed all tadpoles repeatedly for activity and risk-taking both in the absence and presence of olfactory predator stimuli. We found that (a) between-individual variation in predator-induced behavioural plasticity was present only in the group that developed in the presence of olfactory stimuli from predators and (b) previous experience with predatory stimuli resulted in lower plastic response at the group level. The latter pattern resulted from increased between-individual variation and not from universally lower individual responses. We also found that experience with predation during development increased the predictability (i.e. decreased the within-individual variation unrelated to environmental change) of activity, but not risk-taking. In line with this, tadpoles developing under perceived predatory risk expressed their activity with higher repeatability. We suggest that ecologically relevant environmental stimuli are not only fundamental for the development of animal personality and behavioural syndromes, but also for individual variation in behavioural plasticity. Thus, experience is of central importance for the emergence of individual behavioural variation at many levels.

Maternal diet affects juvenile Carpetan rock lizard performance and personality

“…Expressing behavior in an unpredictable way might be an effective antipredator strategy, as predators often rely on predictable patterns in prey locomotion (Briffa, ; Highcock & Carter, ; Richardson, Dickinson, Burman, Pike, & Pike, ). Hence, this pattern is somewhat in line with the predictions of state‐dependent safety principle (Dosmann, Brooks, & Mateo, ; Luttbeg & Sih, ; Sih et al, ), where individuals with low climbing speed suffer higher predation risk while being active and should thus be less predictable (but see Urszán et al, ).…”

“…Although “animal personality research” is one of the fastest developing fields of behavioral ecology, studies on the evolutionary importance of within‐individual behavioral variability started to accumulate only recently (Araya‐Ajoy & Dingemanse, ; Dingemanse, Kazem, Réale, & Wright, ; Stamps, Briffa, & Biro, ). Several studies demonstrated lately that components of within‐individual variation, known as behavioral plasticity (behavioral response induced by environmental change) and behavioral predictability (behavioral variation independent from environmental change), are not only integrated into an individual's behavioral strategy (Chang, Teo, Norma‐Rashid, & Li, ; Lichtenstein, Chism, Kamath, & Pruitt, ; Urszán et al, ; Velasque & Briffa, ), but individual‐specific variation in these components exists (Biro & Adriaenssens, ; Briffa, ; Briffa, Bridger, & Biro, ; Ioannou & Dall, ; Westneat, Wright, & Dingemanse, ). Thus, plasticity and predictability of individual behavior are potentially independent traits, which may be targeted by selection directly (Brembs, ; Mathot & Dingemanse, ).…”

“…Among the standard theories interpreting the emergence of interindividual behavioral variation, state dependence implies the role of individual state differences in creating behavioral consistencies (Bijleveld et al, ; Dall, Houston, & McNamara, ; Rands, Cowlishaw, Pettifor, Rowcliffe, & Johnstone, ; Sih et al, ). Recent empirical data suggest that not only inherently stable (e.g., gender, morphology; see Sih et al, ), but even labile state variables and/or short‐term differences in environmental conditions can shape behavioral consistency (DiRienzo, Niemelä, Hedrick, & Kortet, ; Horváth, Martín, López, Garamszegi, & Herczeg, ; Horváth, Mészáros, et al, ; Lichtenstein et al, ; Urszán, Garamszegi, et al, ; Urszán et al, ; Urszán, Török, Hettyey, Garamszegi, & Herczeg, ). Such variation can have particularly strong effects during early stages of ontogeny (Dingemanse et al, ; DiRienzo & Montiglio, ; Urszán et al, ), but they are also expected to create long‐lasting effects (DiRienzo, Niemelä, Skog, Vainikka, & Kortet, ; DiRienzo, Pruitt, & Hedrick, ; Krause, Krüger, & Schielzeth, ).…”

Brain size predicts behavioural plasticity in guppies (Poecilia reticulata): An experiment

“…animal personality and behavioural syndromes) on/off in adult animals. Further, it is also known that ontogenetic experience with relevant ecological stimuli is needed for the development of between‐individual variation in mean behaviour and behavioural plasticity (Urszán, Garamszegi, et al., ; Urszán et al., ; Urszán, Török, Hettyey, Garamszegi, & Herczeg, ). Based on the observed flexibility of behavioural consistency within populations, we expected to see some variation in the strength of animal personality and presence/absence of between‐individual variation in behavioural plasticity between sexes and/or brain lines.…”

“…Tollrian & Harvell, 1999). However, the fact that the strength of behavioural plasticity varies between individuals; for instance, individuals in a population differ in how much shier they become under perceived predation risk, has only became realized lately both in theoretical (Dingemanse et al, 2010;Dingemanse & Wolf, 2013; and empirical studies (Briffa et al, 2013;Dingemanse, Barber, et al, 2012;Dingemanse, Bouwman, et al, 2012;Porlier et al, 2012;Quinn et al, 2012;Urszán et al, 2018;Westneat et al, 2011). Since it has been shown that between-individual differences in behavioural plasticity can be consistent across individuals, or in other words, can be reliable individual traits (Araya-Ajoj & Dingemanse, 2017;Mitchell & Biro, 2017), the question why such individual differences exist emerged.…”