What can whole genome expression data tell us about the ecology and evolution of personality?

Consistent individual differences in behaviour, aka personality, pose several evolutionary questions. For example, it is difficult to explain within-individual consistency in behaviour because behavioural plasticity is often advantageous. In addition, selection erodes heritable behavioural variation that is related to fitness, therefore we wish to know the mechanisms that can maintain between-individual variation in behaviour. In this paper, we argue that whole genome expression data can reveal new insights into the proximate mechanisms underlying personality, as well as its evolutionary consequences. After introducing the basics of whole genome expression analysis, we show how whole genome expression data can be used to understand whether behaviours in different contexts are affected by the same molecular mechanisms. We suggest strategies for using the power of genomics to understand what maintains behavioural variation, to study the evolution of behavioural correlations and to compare personality traits across diverse organisms.     

An explanatory framework for adaptive personality differences

We develop a conceptual framework for the understanding of animal personalities in terms of adaptive evolution. We focus on two basic questions. First, why do behavioural types exhibit limited behavioural plasticity, that is, behavioural correlations both across contexts and over time? Second, how can multiple behavioural types coexist within a single population? We emphasize differences in 'state' among individuals in combination with state-dependent behaviour. Some states are inherently stable and individual differences in such states can explain stable differences in suites of behaviour if it is adaptive to make behaviour in various contexts dependent on such states. Behavioural stability and cross-context correlations in behaviour are more difficult to explain if individual states are potentially more variable. In such cases stable personalities can result from state-dependent behaviour if state and behaviour mutually reinforce each other by feedback mechanisms. We discuss various evolutionary mechanisms for the maintenance of variation (in states and/or behaviour), including frequency-dependent selection, spatial variation with incomplete matching between habitat and phenotype, bet-hedging in a temporally fluctuating environment, and non-equilibrium dynamics. Although state differences are important, we also discuss how social conventions and social signalling can give rise to adaptive personality differences in the absence of state differences.     

Interindividual variability in social insects – proximate causes and ultimate consequences

Individuals within social groups often show consistent differences in behaviour across time and context. Such interindividual differences and the evolutionary challenge they present have recently generated considerable interest. Social insects provide some of the most familiar and spectacular examples of social groups with large interindividual differences. Investigating these within‐group differences has a long research tradition, and behavioural variability among the workers of a colony is increasingly regarded as fundamental for a key feature of social insects: division of labour. The goal of this review is to illustrate what we know about both the proximate mechanisms underlying behavioural variability among the workers of a colony and its ultimate consequences; and to highlight the many open questions in this research field. We begin by reviewing the literature on mechanisms that potentially introduce, maintain, and adjust the behavioural differentiation among workers. We highlight the fact that so far, most studies have focused on behavioural variability based on genetic variability, provided by e.g. multiple mating of the queen, while other mechanisms that may be responsible for the behavioural differentiation among workers have been largely neglected. These include maturational, nutritional and environmental influences. We further discuss how feedback provided by the social environment and learning and experience of adult workers provides potent and little‐explored sources of differentiation. In a second part, we address what is known about the potential benefits and costs of increased behavioural variability within the workers of a colony. We argue that all studies documenting a benefit of variability so far have done so by manipulating genetic variability, and that a direct test of the effect of behavioural variability on colony productivity has yet to be provided. We emphasize that the costs associated with interindividual variability have been largely overlooked, and that a better knowledge of the cost/benefit balance of behavioural variability is crucial for our understanding of the evolution of the mechanisms underlying the social organization of insect societies. We conclude by highlighting what we believe to be promising but little‐explored avenues for future research on how within‐colony variability has evolved and is maintained. We emphasize the need for comparative studies and point out that, so far, most studies on interindividual variability have focused on variability in individual response thresholds, while the significance of variability in other parameters of individual response, such as probability and intensity of the response, has been largely overlooked. We propose that these parameters have important consequences for the colony response. Much more research is needed to understand if and how interindividual variability is modulated in order to benefit division of labour, homeostasis and ultimately colony fitness in social insects.     

The levels of analysis revisited

The term levels of analysis has been used in several ways: to distinguish between ultimate and proximate levels, to categorize different kinds of research questions and to differentiate levels of reductionism. Because questions regarding ultimate function and proximate mechanisms are logically distinct, I suggest that distinguishing between these two levels is the best use of the term. Integrating across levels in research has potential risks, but many benefits. Consideration at one level can help generate novel hypotheses at the other, define categories of behaviour and set criteria that must be addressed. Taking an adaptationist stance thus strengthens research on proximate mechanisms. Similarly, it is critical for researchers studying adaptation and function to have detailed knowledge of proximate mechanisms that may constrain or modulate evolutionary processes. Despite the benefits of integrating across ultimate and proximate levels, failure to clearly identify levels of analysis, and whether or not hypotheses are exclusive alternatives, can create false debates. Such non-alternative hypotheses may occur between or within levels, and are not limited to integrative approaches. In this review, I survey different uses of the term levels of analysis and the benefits of integration, and highlight examples of false debate within and between levels. The best integrative biology reciprocally uses ultimate and proximate hypotheses to generate a more complete understanding of behaviour.     

Opening the Black Box of Developmental Experiments: Behavioural Mechanisms Underlying Long‐Term Effects of Early Social Experience

Typically, animals spend a considerable portion of their time with social interactions involving mates, offspring, competitors and group members. The social performance during these interactions can strongly depend on the social environment individuals have experienced early in life. Despite a considerable number of experiments investigating long‐term effects of the early social environment, our understanding of the behavioural mechanisms mediating these effects is still limited, mainly for two reasons. (1) Only in few experimental studies have researchers actually observed and quantified the behaviour of their study animals during the social treatment. (2) Even if differences in social interactions between social rearing treatments are reported, these differences might not be causally linked to any observed long‐term effects later in life. The aim of this review was to investigate whether behavioural records of animals during the experimental manipulation of their social environment can help (1) identifying behavioural mechanisms involved in a long‐term effect and (2) obtaining a better understanding of the long‐term consequences of early manipulations. First, I review studies that manipulated the social environment at an early stage of the ontogeny, observed the social interactions and behaviour during the social experience phase and subsequently tested the performance in social and non‐social behavioural tasks at a later life stage. In all reviewed studies, treatment differences were reported both in social interactions during the social experience phase and in social and/or non‐social behaviours later in life. Second, I discuss four classes of behavioural mechanisms that can cause the reported long‐term effects of social experience, namely learning by experience, social learning, sensory stimulation and social cueing. I conclude that social interactions during the social experience phase should always be recorded for at least two reasons. Knowledge about how the social interactions differ between rearing treatments (1) permits researchers to formulate hypotheses about candidate mechanisms causing long‐term effects on behaviour and (2) can help to interpret unexpected outcomes of developmental experiments. Finally, I propose that as a crucial ultimate step towards understanding effects of the early social environment, we should develop targeted experiments testing for the causality of identified candidate mechanism.     

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.     

Behavioural biology: an effective and relevant conservation tool

'Conservation behaviour' is a young discipline that investigates how proximate and ultimate aspects of the behaviour of an animal can be of value in preventing the loss of biodiversity. Rumours of its demise are unfounded. Conservation behaviour is quickly building a capacity to positively influence environmental decision making. The theoretical framework used by animal behaviourists is uniquely valuable to elucidating integrative solutions to human-wildlife conflicts, efforts to reintroduce endangered species and reducing the deleterious effects of ecotourism. Conservation behaviourists must join with other scientists under the multidisciplinary umbrella of conservation biology without giving up on their focus: the mechanisms, development, function and evolutionary history of individual differences in behaviour. Conservation behaviour is an increasingly relevant tool in the preservation of nature.     

Looking for sexual selection in the female brain

Female mate choice behaviour has significant evolutionary consequences, yet its mechanistic origins are not fully understood. Recent studies of female sensory systems have made great strides in identifying internal mechanisms governing female preferences. Only recently, however, have we begun to identify the dynamic genomic response associated with mate choice behaviour. Poeciliids provide a powerful comparative system to examine genomic responses governing mate choice and female preference behaviour, given the great range of mating systems: from female mate choice taxa with ornamental courting males to species lacking male ornamentation and exhibiting only male coercion. Furthermore, they exhibit laboratory-tractable preference responses without sexual contact that are decoupled from reproductive state, allowing investigators to isolate mechanisms in the brain without physiological confounds. Early investigations with poeciliid species (Xiphophorus nigrensis and Gambusia affinis) have identified putative candidate genes associated with female preference response and highlight a possible genomic pathway underlying female social interactions with males linked functionally with synaptic plasticity and learning processes. This network is positively correlated with female preference behaviour in the female mate choice species, but appears inhibited in the male coercive species. This behavioural genomics approach provides opportunity to elucidate the fundamental building blocks, and evolutionary dynamics, of sexual selection.     

Applying evolutionary anthropology

Evolutionary anthropology provides a powerful theoretical framework for understanding how both current environments and legacies of past selection shape human behavioral diversity. This integrative and pluralistic field, combining ethnographic, demographic, and sociological methods, has provided new insights into the ultimate forces and proximate pathways that guide human adaptation and variation. Here, we present the argument that evolutionary anthropological studies of human behavior also hold great, largely untapped, potential to guide the design, implementation, and evaluation of social and public health policy. Focusing on the key anthropological themes of reproduction, production, and distribution we highlight classic and recent research demonstrating the value of an evolutionary perspective to improving human well‐being. The challenge now comes in transforming relevance into action and, for that, evolutionary behavioral anthropologists will need to forge deeper connections with other applied social scientists and policy‐makers. We are hopeful that these developments are underway and that, with the current tide of enthusiasm for evidence‐based approaches to policy, evolutionary anthropology is well positioned to make a strong contribution.     

Social structure modulates the evolutionary consequences of social plasticity: A social network perspective on interacting phenotypes

Organisms express phenotypic plasticity during social interactions. Interacting phenotype theory has explored the consequences of social plasticity for evolution, but it is unclear how this theory applies to complex social structures. We adapt interacting phenotype models to general social structures to explore how the number of social connections between individuals and preference for phenotypically similar social partners affect phenotypic variation and evolution. We derive an analytical model that ignores phenotypic feedback and use simulations to test the predictions of this model. We find that adapting previous models to more general social structures does not alter their general conclusions but generates insights into the effect of social plasticity and social structure on the maintenance of phenotypic variation and evolution. Contribution of indirect genetic effects to phenotypic variance is highest when interactions occur at intermediate densities and decrease at higher densities, when individuals approach interacting with all group members, homogenizing the social environment across individuals. However, evolutionary response to selection tends to increase at greater network densities as the effects of an individual's genes are amplified through increasing effects on other group members. Preferential associations among similar individuals (homophily) increase both phenotypic variance within groups and evolutionary response to selection. Our results represent a first step in relating social network structure to the expression of social plasticity and evolutionary responses to selection.     

Pheromonal control: reconciling physiological mechanism with signalling theory

Pheromones are intraspecific chemical signals. They can have profound effects on the behaviour and/or physiology of the receiver, and it is still common to hear pheromones described as controlling of the behaviour of the receiver. The discussion of pheromonal control arose initially from a close association between hormones and pheromones in the comparative physiological literature, but the concept of a controlling pheromone is at odds with contemporary signal evolution theory, which predicts that a manipulative pheromonal signal negatively affecting the receiver's fitness should not be stable over evolutionary time. Here we discuss the meaning of pheromonal control, and the ecological circumstances by which it might be supported. We argue that in discussing pheromonal control it is important to differentiate between control applied to the effects of a pheromone on a receiver's physiology (proximate control), and control applied to the effects of a pheromone on a receiver's fitness (ultimate control). Critically, a pheromone signal affecting change in the receiver's behaviour or physiology need not necessarily manipulate the fitness of a receiver. In cases where pheromonal signalling does lead to a reduction in the fitness of the receiver, the signalling system would be stable if the pheromone were an honest signal of a social environment that disadvantages the receiver, and the physiological and behavioural changes observed in the receiver were an adaptive response to the new social circumstances communicated by the pheromone.     

Evolution of multivariate wing allometry in schizophoran flies (Diptera: Schizophora)

The proximate and ultimate mechanisms underlying scaling relationships as well as their evolutionary consequences remain an enigmatic issue in evolutionary biology. Here, I investigate the evolution of wing allometries in the Schizophora, a group of higher Diptera that radiated about 65 million years ago, by studying static allometries in five species using multivariate approaches. Despite the vast ecological diversity observed in contemporary members of the Schizophora and independent evolutionary histories throughout most of the Cenozoic, size‐related changes represent a major contributor to overall variation in wing shape, both within and among species. Static allometries differ between species and sexes, yet multivariate allometries are correlated across species, suggesting a shared developmental programme underlying size‐dependent phenotypic plasticity. Static allometries within species also correlate with evolutionary divergence across 33 different families (belonging to 11 of 13 superfamilies) of the Schizophora. This again points towards a general developmental, genetic or evolutionary mechanism that canalizes or maintains the covariation between shape and size in spite of rapid ecological and morphological diversification during the Cenozoic. I discuss the putative roles of developmental constraints and natural selection in the evolution of wing allometry in the Schizophora.     

Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection

From an evolutionary perspective, social behaviours are those which have fitness consequences for both the individual that performs the behaviour, and another individual. Over the last 43 years, a huge theoretical and empirical literature has developed on this topic. However, progress is often hindered by poor communication between scientists, with different people using the same term to mean different things, or different terms to mean the same thing. This can obscure what is biologically important, and what is not. The potential for such semantic confusion is greatest with interdisciplinary research. Our aim here is to address issues of semantic confusion that have arisen with research on the problem of cooperation. In particular, we: (i) discuss confusion over the terms kin selection, mutualism, mutual benefit, cooperation, altruism, reciprocal altruism, weak altruism, altruistic punishment, strong reciprocity, group selection and direct fitness; (ii) emphasize the need to distinguish between proximate (mechanism) and ultimate (survival value) explanations of behaviours. We draw examples from all areas, but especially recent work on humans and microbes.     

Semiotic Mechanisms Underlying Niche Construction

The explanatory value of niche construction can be strengthened by firm footing in semiotic theory. Anthropologists have a unique perspective on the integration of such diverse approaches to human action and evolutionary processes. Here, we seek to open a dialogue between anthropology and biosemiotics. The overarching aim of this paper is to demonstrate that niche construction, including the underlying mechanism of reciprocal causation, is a semiotic process relating to biological development (sensu stricto) as well as cognitive development and cultural change. In making this argument we emphasize the semiotic mechanisms underlying the niche concept. We argue that the “niche” in ecology and evolutionary biology can be consistent with the Umwelt of Jakob von Uexkull. Following John Deely we therefore suggest that investigations into the organism—environment interface constituting niche construction should emphasize the semiotic basis of experience. Peircean signs are pervasive and allow for flexible interpretations of phenomena in relation to the perceptual and cognitive capacities of the behaving organism, which is particularly pertinent for understanding the relation of proximate/ultimate selective forces as co-productive (i.e., reciprocal). Additionally, theoretical work by Kinji Imanishi on the evolution of daily life and Gregory Bateson’s relational view of evolution both support the linkage between proximate and ultimate evolutionary processes of causation necessitated by the niche construction perspective. We will then apply this theoretical framework to two specific examples: 1) hominin evolution, including uniquely human cultural behaviors with niche constructive implications; and 2) the multispecies and anthropocentric niche of human-dog coevolution from which complex cognitive capacities and semiotic relationships emerged. The intended outcome of this paper is the establishment of concrete semiotic mechanisms and theory underlying niche constructive behavior which can then be applied to a broad spectrum of organisms to contextualize the reciprocal relation between proximate and ultimate drivers of behavior.     

Culture and courtship in vertebrates: a review of social learning and transmission of courtship systems and mating patterns

Female and male animals often choose mates based upon the complementarity of their courtship behaviours and preferences. The importance of this fact on the evolutionary dynamics of populations has long been appreciated. What has not been appreciated is the role that social learning might play in the transmission of systems of courtship behaviour across generations. This paper addresses the social transmission of courtship behavioural traditions in vertebrates. It discusses views of culture in the context of behavioural signals and preferences in courtship. It then reviews empirical evidence for culture-like processes affecting courtship behaviour, focusing on studies of song learning in passerine birds and work on social learning of mating preferences. The paper concludes with potential future directions for research on social traditions in systems of courtship behaviour, including determining mechanisms of transmission, genetic and non-social environmental effects, and selective factors influencing the stability of behavioural traditions over time. By integrating proximate and ultimate questions for the transmission of courtship systems, this work would increase our understanding of the ways individual development, cultural processes, and population evolution influence, and are in turn influenced by, one another.     

Morphology and behaviour: functional links in development and evolution

Development and evolution of animal behaviour and morphology are frequently addressed independently, as reflected in the dichotomy of disciplines dedicated to their study distinguishing object of study (morphology versus behaviour) and perspective (ultimate versus proximate). Although traits are known to develop and evolve semi-independently, they are matched together in development and evolution to produce a unique functional phenotype. Here I highlight similarities shared by both traits, such as the decisive role played by the environment for their ontogeny. Considering the widespread developmental and functional entanglement between both traits, many cases of adaptive evolution are better understood when proximate and ultimate explanations are integrated. A field integrating these perspectives is evolutionary developmental biology (evo-devo), which studies the developmental basis of phenotypic diversity. Ultimate aspects in evo-devo studies--which have mostly focused on morphological traits--could become more apparent when behaviour, 'the integrator of form and function', is integrated into the same framework of analysis. Integrating a trait such as behaviour at a different level in the biological hierarchy will help to better understand not only how behavioural diversity is produced, but also how levels are connected to produce functional phenotypes and how these evolve. A possible framework to accommodate and compare form and function at different levels of the biological hierarchy is outlined. At the end, some methodological issues are discussed.     

Developmental plasticity and the evolution of parental effects

One of the outstanding challenges for evolutionary biologists is to understand how developmental plasticity can influence the evolutionary process. Developmental plasticity frequently involves parental effects, which might enable adaptive and context-dependent transgenerational transmission of phenotypic strategies. However, parent-offspring conflict will frequently result in parental effects that are suboptimal for parents, offspring or both. The fitness consequences of parental effects at evolutionary equilibrium will depend on how conflicts can be resolved by modifications of developmental processes, suggesting that proximate studies of development can inform ultimate questions. Furthermore, recent studies of plants and animals show how studies of parental effects in an ecological context provide important insights into the origin and evolution of adaptation under variable environmental conditions.     

Beyond the phenotypic gambit: molecular behavioural ecology and the evolution of genetic architecture

Most studies of behaviour examine traits whose proximate causes include sensory input and neural decision-making, but conflict and collaboration in biological systems began long before brains or sensory systems evolved. Many behaviours result from non-neural mechanisms such as direct physical contact between recognition proteins or modifications of development that coincide with altered behaviour. These simple molecular mechanisms form the basis of important biological functions and can enact organismal interactions that are as subtle, strategic and interesting as any. The genetic changes that underlie divergent molecular behaviours are often targets of selection, indicating that their functional variation has important fitness consequences. These behaviours evolve by discrete units of quantifiable phenotypic effect (amino acid and regulatory mutations, often by successive mutations of the same gene), so the role of selection in shaping evolutionary change can be evaluated on the scale at which heritable phenotypic variation originates. We describe experimental strategies for finding genes that underlie biochemical and developmental alterations of behaviour, survey the existing literature highlighting cases where the simplicity of molecular behaviours has allowed insight to the evolutionary process and discuss the utility of a genetic knowledge of the sources and spectrum of phenotypic variation for a deeper understanding of how genetic and phenotypic architectures evolve.     

Social brains,simple minds: does social complexity really require cognitive complexity?

The social brain hypothesis is a well-accepted and well-supported evolutionary theory of enlarged brain size in the non-human primates. Nevertheless, it tends to emphasize an anthropocentric view of social life and cognition. This often leads to confusion between ultimate and proximate mechanisms, and an over-reliance on a Cartesian, narratively structured view of the mind and social life, which in turn lead to views of social complexity that are congenial to our views of ourselves, rather than necessarily representative of primate social worlds. In this paper, we argue for greater attention to embodied and distributed theories of cognition, which get us away from current fixations on 'theory of mind' and other high-level anthropocentric constructions, and allow for the generation of testable hypotheses that combine neurobiology, psychology and behaviour in a mutually reinforcing manner.     

Macro-evolutionary studies of cultural diversity: a review of empirical studies of cultural transmission and cultural adaptation

A growing body of theoretical and empirical research has examined cultural transmission and adaptive cultural behaviour at the individual, within-group level. However, relatively few studies have tried to examine proximate transmission or test ultimate adaptive hypotheses about behavioural or cultural diversity at a between-societies macro-level. In both the history of anthropology and in present-day work, a common approach to examining adaptive behaviour at the macro-level has been through correlating various cultural traits with features of ecology. We discuss some difficulties with simple ecological associations, and then review cultural phylogenetic studies that have attempted to go beyond correlations to understand the underlying cultural evolutionary processes. We conclude with an example of a phylogenetically controlled approach to understanding proximate transmission pathways in Austronesian cultural diversity.