Time-specific convergence and divergence in individual differences in behavior: Theory, protocols and analyzes.

Over the years, theoreticians and empiricists working in a wide range of disciplines, including physiology, ethology, psychology, and behavioral ecology, have suggested a variety of reasons why individual differences in behavior might change over time, such that different individuals become more similar (convergence) or less similar (divergence) to one another. Virtually none of these investigators have suggested that convergence or divergence will continue forever, instead proposing that these patterns will be restricted to particular periods over the course of a longer study. However, to date, few empiricists have documented time-specific convergence or divergence, in part because the experimental designs and statistical methods suitable for describing these patterns are not widely known. Here, we begin by reviewing an array of influential hypotheses that predict convergence or divergence in individual differences over timescales ranging from minutes to years, and that suggest how and why such patterns are likely to change over time (e.g., divergence followed by maintenance). Then, we describe experimental designs and statistical methods that can be used to determine if (and when) individual differences converged, diverged, or were maintained at the same level at specific periods during a longitudinal study. Finally, we describe why the concepts described herein help explain the discrepancy between what theoreticians and empiricists mean when they describe the "emergence" of individual differences or personality, how they might be used to study situations in which convergence and divergence patterns alternate over time, and how they might be used to study time-specific changes in other attributes of behavior, including individual differences in intraindividual variability (predictability), or genotypic differences in behavior.

Combining information from parental and personal experiences: Simple processes generate diverse outcomes.

Experiences of parents and/or offspring are often assumed to affect the development of trait values in offspring because they provide information about the external environment. However, it is currently unclear how information from parental and offspring experiences might jointly affect the information-states that provide the foundation for the offspring phenotypes observed in empirical studies of developmental plasticity in response to environmental cues. We analyze Bayesian models designed to mimic fully-factorial experimental studies of trans and within- generational plasticity (TWP), in which parents, offspring, both or neither are exposed to cues from predators, to determine how different durations of cue exposure for parents and offspring, the devaluation of information from parents or the degradation of information from parents would affect offspring estimates of environmental states related to risk of predation at the end of such experiments. We show that the effects of different cue durations, the devaluation of information from parents, and the degradation of information from parents on offspring estimates are all expected to vary as a function of interactions with two other key components of information-based models of TWP: parental priors and the relative cue reliability in the different treatments. Our results suggest empiricists should expect to observe considerable variation in the patterns observed in experimental studies of TWP based on simple principles of information-updating, without needing to invoke additional assumptions about costs, tradeoffs, development constraints, the fitness consequences of different trait values, or other factors.

The information provided by the absence of cues: insights from Bayesian models of within and transgenerational plasticity.

Empirical studies of phenotypic plasticity often use an experimental design in which the subjects in experimental treatments are exposed to cues, while the subjects in control treatments are maintained in the absence of those cues. However, researchers have virtually ignored the question of what, if any, information might be provided to subjects by the absence of the cues in control treatments. We apply basic principles of information-updating to several experimental protocols used to study phenotypic plasticity in response to cues from predators to show why the reliability of the information provided by the absence of those cues in a control treatment might vary as a function of the subjects' experiences in the experimental treatment. We then analyze Bayesian models designed to mimic fully factorial experimental studies of trans and within-generational plasticity, in which parents, offspring, both or neither are exposed to cues from predators, and the information-states of the offspring in the different groups are compared at the end of the experiment. The models predict that the pattern of differences in offspring information-state across the four treatment groups will vary among experiments, depending on the reliability of the information provided by the control treatment, and the parent's initial estimate of the value of the state (the parental Prior). We suggest that variation among experiments in the reliability of the information provided by the absence of particular cues in the control treatment may be a general phenomenon, and that Bayesian approaches can be useful in interpreting the results of such experiments.

Bayesian updating during development predicts genotypic differences in plasticity.

Interactions between genotypes and environments are central to evolutionary genetics, but such interactions are typically described, rather than predicted from theory. Recent Bayesian models of development generate specific predictions about genotypic differences in developmental plasticity (changes in the value of a given trait as a result of a given experience) based on genotypic differences in the value of the trait that is expressed by naïve subjects. We used these models to make a priori predictions about the effects of an aversive olfactory conditioning regime on the response of Drosophila melanogaster larvae to the odor of ethyl acetate. As predicted, across 116 genotypes initial trait values were related to plasticity. Genotypes most strongly attracted to the odor of ethyl acetate when naïve reduced their attraction scores more as a result of the aversive training regime than those less attracted to the same odor when naïve. Thus, as predicted, the variance across genotypes in attraction scores was higher before than after the shared experience. These results support predictions generated by Bayesian models of development and indicate that such models can be successfully used to investigate how variation across genotypes in information derived from ancestors combines with personal experience to differentially affect developmental plasticity in response to specific types of experience.

Bayesian Models of Development.

Until recently, biology lacked a framework for studying how information from genes, parental effects, and different personal experiences is combined across the lifetime to affect phenotypic development. Over the past few years, researchers have begun to build such a framework, using models that incorporate Bayesian updating to study the evolution of developmental plasticity and developmental trajectories. Here, we describe the merits of a Bayesian approach to development, review the main findings and implications of the current set of models, and describe predictions that can be tested using protocols already used by empiricists. We suggest that a Bayesian perspective affords a simple and tractable way to conceptualize, explain, and predict how information combines across the lifetime to affect development.

Individual differences in behavioural plasticities.

Interest in individual differences in animal behavioural plasticities has surged in recent years, but research in this area has been hampered by semantic confusion as different investigators use the same terms (e.g. plasticity, flexibility, responsiveness) to refer to different phenomena. The first goal of this review is to suggest a framework for categorizing the many different types of behavioural plasticities, describe examples of each, and indicate why using reversibility as a criterion for categorizing behavioural plasticities is problematic. This framework is then used to address a number of timely questions about individual differences in behavioural plasticities. One set of questions concerns the experimental designs that can be used to study individual differences in various types of behavioural plasticities. Although within-individual designs are the default option for empirical studies of many types of behavioural plasticities, in some situations (e.g. when experience at an early age affects the behaviour expressed at subsequent ages), 'replicate individual' designs can provide useful insights into individual differences in behavioural plasticities. To date, researchers using within-individual and replicate individual designs have documented individual differences in all of the major categories of behavioural plasticities described herein. Another important question is whether and how different types of behavioural plasticities are related to one another. Currently there is empirical evidence that many behavioural plasticities [e.g. contextual plasticity, learning rates, IIV (intra-individual variability), endogenous plasticities, ontogenetic plasticities) can themselves vary as a function of experiences earlier in life, that is, many types of behavioural plasticity are themselves developmentally plastic. These findings support the assumption that differences among individuals in prior experiences may contribute to individual differences in behavioural plasticities observed at a given age. Several authors have predicted correlations across individuals between different types of behavioural plasticities, i.e. that some individuals will be generally more plastic than others. However, empirical support for most of these predictions, including indirect evidence from studies of relationships between personality traits and plasticities, is currently sparse and equivocal. The final section of this review suggests how an appreciation of the similarities and differences between different types of behavioural plasticities may help theoreticians formulate testable models to explain the evolution of individual differences in behavioural plasticities and the evolutionary and ecological consequences of individual differences in behavioural plasticities.

Combining information from ancestors and personal experiences to predict individual differences in developmental trajectories.

A persistent question in biology is how information from ancestors combines with personal experiences over the lifetime to affect the developmental trajectories of phenotypic traits. We address this question by modeling individual differences in behavioral developmental trajectories on the basis of two assumptions: (1) differences among individuals in the behavior expressed at birth or hatching are based on information from their ancestors (via genes, epigenes, and prenatal maternal effects), and (2) information from ancestors is combined with information from personal experiences over ontogeny via Bayesian updating. The model predicts relationships between the means and the variability of the behavior expressed by neonates and the subsequent developmental trajectories of their behavior when every individual is reared under the same environmental conditions. Several predictions of the model are supported by data from previous studies of behavioral development, for example, that the temporal stability of personality will increase with age and that the intercepts and slopes of developmental trajectories for boldness will be negatively correlated across individuals or genotypes when subjects are raised in safe environments. We describe how other specific predictions of the model can be used to test the hypothesis that information from ancestors and information from personal experiences are combined via nonadditive, Bayesian-like processes.

Genotypic differences in behavioural entropy: unpredictable genotypes are composed of unpredictable individuals.

Intra-genotypic variability (IGV) occurs when individuals with the same genotype, raised in the same environment and then tested under the same conditions, express different trait values. Game theoretical and bet-hedging models have suggested two ways that a single genotype might generate variable behaviour when behavioural variation is discrete rather than continuous: behavioural polyphenism (a genotype produces different types of individuals, each of which consistently expresses a different type of behaviour) or stochastic variability (a genotype produces one type of individual who randomly expresses different types of behaviour over time). We first demonstrated significant differences across 14 natural genotypes of male Drosophila melanogaster in the variability (as measured by entropy) of their microhabitat choice, in an experiment in which each fly was allowed free access to four different types of habitat. We then tested four hypotheses about ways that within-individual variability might contribute to differences across genotypes in the variability of microhabitat choice. There was no empirical support for three hypotheses (behavioural polymorphism, consistent choice, or time-based choice), nor could our results be attributed to genotypic differences in activity levels. The stochastic variability hypothesis accurately predicted the slope and the intercept of the relationship across genotypes between entropy at the individual level and entropy at the genotype level. However, our initial version of the stochastic model slightly but significantly overestimated the values of individual entropy for each genotype, pointing to specific assumptions of this model that might need to be adjusted in future studies of the IGV of microhabitat choice. This is among a handful of recent studies to document genotypic differences in behavioural IGV, and the first to explore ways that genotypic differences in within-individual variability might contribute to differences among genotypes in the predictability of their behaviour.

Drosophila regulate yeast density and increase yeast community similarity in a natural substrate.

Drosophila melanogaster adults and larvae, but especially larvae, had profound effects on the densities and community structure of yeasts that developed in banana fruits. Pieces of fruit exposed to adult female flies previously fed fly-conditioned bananas developed higher yeast densities than pieces of the same fruits that were not exposed to flies, supporting previous suggestions that adult Drosophila vector yeasts to new substrates. However, larvae alone had dramatic effects on yeast density and species composition. When yeast densities were compared in pieces of the same fruits assigned to different treatments, fruits that developed low yeast densities in the absence of flies developed significantly higher yeast densities when exposed to larvae. Across all of the fruits, larvae regulated yeast densities within narrow limits, as compared to a much wider range of yeast densities that developed in pieces of the same fruits not exposed to flies. Larvae also affected yeast species composition, dramatically reducing species diversity across fruits, reducing variation in yeast communities from one fruit to the next (beta diversity), and encouraging the consistent development of a yeast community composed of three species of yeast (Candida californica, C. zemplinina, and Pichia kluvyeri), all of which were palatable to larvae. Larvae excreted viable cells of these three yeast species in their fecal pools, and discouraged the growth of filamentous fungi, processes which may have contributed to their effects on the yeast communities in banana fruits. These and other findings suggest that D. melanogaster adults and their larval offspring together engage in 'niche construction', facilitating a predictable microbial environment in the fruit substrates in which the larvae live and develop.

Developmental perspectives on personality: implications for ecological and evolutionary studies of individual differences.

Developmental processes can have major impacts on the correlations in behaviour across contexts (contextual generality) and across time (temporal consistency) that are the hallmarks of animal personality. Personality can and does change: at any given age or life stage it is contingent upon a wide range of experiential factors that occurred earlier in life, from prior to conception through adulthood. We show how developmental reaction norms that describe the effects of prior experience on a given behaviour can be used to determine whether the effects of a given experience at a given age will affect contextual generality at a later age, and to illustrate how variation within individuals in developmental plasticity leads to variation in contextual generality across individuals as a function of experience. We also show why niche-picking and niche-construction, behavioural processes which allow individuals to affect their own developmental environment, can affect the contextual generality and the temporal consistency of personality. We conclude by discussing how an appreciation of developmental processes can alert behavioural ecologists studying animal personality to critical, untested assumptions that underlie their own research programmes, and outline situations in which a developmental perspective can improve studies of the functional significance and evolution of animal personality.

Do consistent individual differences in metabolic rate promote consistent individual differences in behavior?

Consistent individual differences (CIDs) in behavior are a widespread phenomenon in animals, but the proximate reasons for them are unresolved. We discuss evidence for the hypothesis that CIDs in energy metabolism, as reflected by resting metabolic rate (RMR), promote CIDs in behavior patterns that either provide net energy (e.g. foraging activity), and/or consume energy (e.g. courtship activity). In doing so, we provide a framework for linking together RMR, behavior, and life-history productivity. Empirical studies suggest that RMR is (a) related to the capacity to generate energy, (b) repeatable, and (c) correlated with behavioral output (e.g. aggressiveness) and productivity (e.g. growth). We conclude by discussing future research directions to clarify linkages between behavior and energy metabolism in this emerging research area.

Adaptation and plasticity of animal communication in fluctuating environments.

Adaptations that facilitate the reception of long-range signals under challenging conditions are expected to generate signal diversity when species communicate in different habitats. Although we have a general understanding of how individual communicating animals cope with conditions influencing signal detection, the extent to which plasticity and evolutionary changes in signal characteristics contribute to interspecific differences in signaling behavior is unclear. We quantified the visual displays of free-living lizards and environmental variables known to influence display detection for multiple species from two separate island radiations. We found evidence of both adaptive evolution and adaptive plasticity in display characteristics as a function of environmental conditions, but plasticity accounted for most of the observed differences in display behavior across species. At the same time, prominent differences between the two island radiations existed in aspects of signaling behavior, unrelated to the environment. Past evolutionary events have therefore played an important role in shaping the way lizards adjust their signals to challenges in present-day environments. In addition to showing how plasticity contributes to interspecific differences in communication signals, our findings suggest the vagaries of evolution can in itself lead to signal variation between species.

Behavior as a key component of integrative biology in a human-altered world.

A major grand challenge in biology is to understand the interactions between an organism and its environment. Behavior resides in the central core of this association as it affects and is affected by development, physiology, ecological dynamics, environmental choice, and evolution. We present this central role of behavior in a diagram illustrating the multifaceted program emphasizing the necessity for understanding this nexus and to fully appreciate the organism in its environment given the ongoing changes affected by contemporary human induced, rapid environmental change (HIREC). We call for the consideration of educational and research focuses to concentrate on the interdisciplinary role that behavior plays in the integration of biological processes.

The development of animal personality: relevance, concepts and perspectives.

Recent studies of animal personality have focused on its proximate causation and its ecological and evolutionary significance, but have mostly ignored questions about its development, although an understanding of the latter is highly relevant to these other questions. One possible reason for this neglect is confusion about many of the concepts and terms that are necessary to study the development of animal personality. Here, we provide a framework for studying personality development that focuses on the properties of animal personality, and considers how and why these properties may change over time. We specifically focus on three dimensions of personality: (1) contextual generality at a given age or time, (2) temporal consistency in behavioural traits and in relationships between traits, and (3) the effects of genes and experience on the development of personality at a given age or life stage. We advocate using a new approach, contextual reaction norms, to study the contextual generality of personality traits at the level of groups, individuals and genotypes, show how concepts and terms borrowed from the literature on personality development in humans can be used to study temporal changes in personality at the level of groups and individuals, and demonstrate how classical developmental reaction norms can provide insights into the ways that genes and experiential factors interact across ontogeny to affect the expression of personality traits. In addition, we discuss how correlations between the effects of genes and experience on personality development can arise as a function of individuals' control over their own environment, via niche-picking or niche-construction. Using this framework, we discuss several widely held assumptions about animal personality development that still await validation, identify neglected methodological issues, and describe a number of promising new avenues for future research.

Small within-day increases in temperature affects boldness and alters personality in coral reef fish.

Consistent individual differences in behaviour, termed personality, are common in animal populations and can constrain their responses to ecological and environmental variation, such as temperature. Here, we show for the first time that normal within-daytime fluctuations in temperature of less than 3 degrees C have large effects on personality for two species of juvenile coral reef fish in both observational and manipulative experiments. On average, individual scores on three personality traits (PTs), activity, boldness and aggressiveness, increased from 2.5- to sixfold as a function of temperature. However, whereas most individuals became more active, aggressive and bold across temperature contexts (were plastic), others did not; this changed the individual rank order across temperatures and thus altered personality. In addition, correlations between PTs were consistent across temperature contexts, e.g. fish that were active at a given temperature also tended to be both bold and aggressive. These results (i) highlight the importance of very carefully controlling for temperature when studying behavioural variation among and within individuals and (ii) suggest that individual differences in energy metabolism may contribute to animal personality, given that temperature has large direct effects on metabolic rates in ectotherms.

How different types of natal experience affect habitat preference.

In many animals, exposure to cues in a natal habitat increases disperser preferences for those cues (natal habitat preference induction [NHPI]), but the proximate and ultimate bases for this phenomenon are obscure. We developed a Bayesian model to study how different types of experience in the natal habitat and survival to the age/stage of dispersal interact to affect a disperser's estimate of the quality of new natal-type habitats. The model predicts that the types of experience a disperser had before leaving its natal habitat will affect the attractiveness of cues from new natal-type habitats and that favorable experiences will increase the level of preference for natal-type habitats more than unfavorable experiences will decrease it. An experimental study of NHPI in Drosophila melanogaster provided with "good" and "bad" experiences in their natal habitats supports these predictions while also indicating that the effects of different types of natal experience on NHPI vary across genotypes. If habitat preferences are modulated by an individual's experience before dispersal as described in this study, then NHPI may have stronger effects on sympatric speciation, metapopulation dynamics, conservation biology, and pest management than previously supposed.

Species identity cues in animal communication.

Researchers have suggested that animals should respond more strongly to conspecific than to heterospecific communication signals used in territorial or courtship contexts. We tested this prediction by reviewing studies that appeared in six prominent journals over the past 10 years. A meta-analysis based on these empirical studies revealed that overall support for this hypothesis was weaker than anticipated. To help clarify the extent to which experimental design might contribute to equivocal findings, we performed playback experiments in the field, using robotic lizards. We examined whether male tropical lizards, Anolis gundlachi, responded more strongly to robots producing conspecific territorial advertisement displays than to robots producing equivalent displays of a novel heterospecific. Although this experiment was conducted under natural conditions in the field, at signaler-receiver distances typical for animals at this locality, and with high statistical power, we found that lizards responded just as aggressively to a simulated rival performing a display they had never seen before as to the same rival performing a conspecific display. Our findings suggest that predicting how animals will respond to conspecific versus heterospecific signals is more complicated than has generally been anticipated.

Effects of survival on the attractiveness of cues to natal dispersers.

Habitat selection by natal dispersers is one of several contexts in which preexisting biases interact with experience to affect the attractiveness of cues from biologically significant items. Here we use a Bayesian approach to explore the conditions that favor this phenomenon. We demonstrate that the simplest possible type of natal experience--namely, survival to the age/stage of dispersal--can increase the attractiveness of cues from an individual's natal habitat relative to the attractiveness of those same cues to naive individuals. The effects of survivorship on cue attractiveness are strongest when the quality of the habitat that produces that cue varies widely across large spatial or temporal scales, when that type of habitat is rarely of high quality, and when offspring survivorship provides a reliable indication of the quality of that type of habitat at the current time and locality. More generally, the framework outlined here may also apply to other situations in which extended exposure to cues early in life increases the attractiveness of those cues later in life.

Alert signals enhance animal communication in "noisy" environments.

Environmental noise that reduces the probability that animals will detect communicative signals poses a special challenge for long-range communication. The application of signal-detection theory to animal communication lead to the prediction that signals directed at distant receivers in noisy environments will begin with conspicuous "alerting" components to attract the attention of receivers, before delivery of the information-rich portion of the signal. Whether animals actually adopt this strategy is not clear, despite suggestions that alerts might exist in a variety of taxa. By using a combination of behavioral observations and experimental manipulations with robotic lizard "playbacks," we show that free-living territorial Anolis lizards add an "alert" to visual displays when communicating to distant receivers in situations of poor visibility, and that these introductory alerts in turn enhance signal detection in adverse signaling conditions. Our results show that Anolis lizards are able to evaluate environmental conditions that affect the degradation of long-distance signals and adjust their behavior accordingly. This study demonstrates that free-living animals enhance the efficiency of long-range communication through the modulation of signal design and the facultative addition of an alert. Our findings confirm that alert signals are an important strategy for communicating in "noisy" conditions and suggest a reexamination of the existence of alerts in other animals relying on long-range communication.

Searching for a new home: decision making by dispersing brush mice.

Natal dispersal occurs when young animals leave the area where they were born and reared and search the surrounding landscape for a new place to settle. Despite the importance of dispersal for both individuals and populations, search behavior by dispersers, including the decision-making process of choosing a place to settle, has not been investigated in the field. Here we draw on the mate search literature, in which the theory of decision making during search has been well developed, and ask whether there are behavioral similarities between habitat search and mate search. We used radiotelemetry to track dispersing juvenile brush mice (Peromyscus boylii) and determined whether their search behavior was consistent with any of three decision rules: threshold, best of n, and comparative Bayes. We found that search behavior by juveniles was most often consistent with comparative decision rules (best of n and comparative Bayes), suggesting that the decision-making processes involved in searching for a place to settle and searching for a mate may be quite similar.