Yimen Gerardo Araya-Ajoy

Characterizing behavioural ‘characters’: an evolutionary framework

Biologists often study phenotypic evolution assuming that phenotypes consist of a set of quasi-independent units that have been shaped by selection to accomplish a particular function. In the evolutionary literature, such quasi-independent functional units are called ‘evolutionary characters’, and a framework based on evolutionary principles has been developed to characterize them. This framework mainly focuses on ‘fixed’ characters, i.e. those that vary exclusively between individuals. In this paper, we introduce multi-level variation and thereby expand the framework to labile characters, focusing on behaviour as a worked example. We first propose a concept of ‘behavioural characters’ based on the original evolutionary character concept. We then detail how integration of variation between individuals (cf. ‘personality’) and within individuals (cf. ‘individual plasticity’) into the framework gives rise to a whole suite of novel testable predictions about the evolutionary character concept. We further propose a corresponding statistical methodology to test whether observed behaviours should be considered expressions of a hypothesized evolutionary character. We illustrate the application of our framework by characterizing the behavioural character ‘aggressiveness’ in wild great tits, Parus major.

Parental provisioning behaviour plays a key role in linking personality with reproductive success

Repeatable behavioural traits (‘personality’) have been shown to covary with fitness, but it remains poorly understood how such behaviour–fitness relationships come about. We applied a multivariate approach to reveal the mechanistic pathways by which variation in exploratory and aggressive behaviour is translated into variation in reproductive success in a natural population of blue tits, Cyanistes caeruleus. Using path analysis, we demonstrate a key role for provisioning behaviour in mediating the link between personality and reproductive success (number of fledged offspring). Aggressive males fed their nestlings at lower rates than less aggressive individuals. At the same time, their low parental investment was associated with increased female effort, thereby positively affecting fledgling production. Whereas male exploratory behaviour was unrelated to provisioning behaviour and reproductive success, fast-exploring females fed their offspring at higher rates and initiated breeding earlier, thus increasing reproductive success. Our findings provide strong support for specific mechanistic pathways linking components of behavioural syndromes to reproductive success. Importantly, relationships between behavioural phenotypes and reproductive success were obscured when considering simple bivariate relationships, underlining the importance of adopting multivariate views and statistical tools as path analysis to the study of behavioural evolution.

Does metabolic rate predict risk-taking behaviour?: A field experiment in a wild passerine bird

Summary Individuals often show consistent differences in risk-taking behaviours; behaviours that increase resource acquisition at the expense of an increased risk of mortality. Recently, basal metabolic rate (BMR) has been suggested as a potentially important state variable underlying adaptive individual differences in a range of behaviours, including risk-taking. We tested the relationship between BMR and risk-taking in free-living great tits (Parus major) using experimental manipulations of perceived predation risk. We compared the latency of individuals to return to feeders following control (human) and predator (model sparrowhawk, Accipiter nisus) disturbances at fixed feeder locations. We predicted that if variation in risk-taking is shaped by energetic constraints, high BMR individuals should return to feeders sooner following both disturbance types and show smaller changes in risk-taking as a function of predation danger. Higher BMR tended to be associated with lower risk-taking following control disturbances but greater risk-taking following predator disturbances, resulting in a significant interaction between BMR and treatment. Within-individual changes in risk-taking as a function of ambient temperature (a proxy for within-individual changes in energetic constraints) mirrored these results. Lower temperatures tended to be associated with lower risk-taking following control disturbances, but greater risk-taking following predator disturbances, resulting in a significant interaction between temperature and treatment. The effects of BMR and temperature on variation in risk-taking as a function of perceived predation danger were qualitatively similar, suggesting that energetic constraints play a role in shaping risk-taking. However, the hypothesized mechanism (energetic requirements directly influence the optimal expression of risk-taking behaviour) is insufficient to account for the observed negative relationship between energetic constraint and risk-taking following control disturbances. We conclude that variation in risk-taking is associated with differences in energetic constraints, including BMR and temperature, but that the relationship is context-specific, here high vs. low perceived predation risk. Further studies are needed to elucidate potential mechanisms that could generate context-specific relationships between energetic constraints and risk-taking.

An approach to estimate short-term, long-term, and reaction norm repeatability

Evolutionary ecologists increasingly study reaction norms that are expressed repeatedly within the same individuals lifetime. For example, foragers continuously alter anti-predator vigilance in response to moment-to-moment changes in predation risk. Variation in this form of plasticity occurs both among and within individuals. Among-individual variation in plasticity (individual by environment interaction or I × E) is commonly studied; by contrast, despite increasing interest in its evolution and ecology, within-individual variation in phenotypic plasticity is not. We outline a study design based on repeated measures and a multilevel extension of random regression models that enables quantification of variation in reaction norms at different hierarchical levels (such as among and within individuals). The approach enables the calculation of repeatability of reaction norm intercepts (average phenotype) and slopes (level of phenotypic plasticity); these indices are not specific to measurement or scaling and are readily comparable across data sets. The proposed study design also enables calculation of repeatability at different temporal scales (such as short- and long-term repeatability), thereby answering calls for the development of approaches enabling scale-dependent repeatability calculations. We introduce a simulation package in the R statistical language to assess power, imprecision and bias for multilevel random regression that may be utilised for realistic data sets (unequal sample sizes across individuals, missing data, etc). We apply the idea to a worked example to illustrate its utility. We conclude that consideration of multilevel variation in reaction norms deepens our understanding of the hierarchical structuring of labile characters and helps reveal the biology in heterogeneous patterns of within-individual variance that would otherwise remain ‘unexplained’ residual variance.

Does coping style predict optimization? An experimental test in a wild passerine bird

A number of studies have suggested that avian brood size is individually optimized. Yet, optimal reproductive decisions likely vary owing to among-individual differences in environmental sensitivity. Specifically, ‘proactive’ individuals who do not track environmental changes may be less able to produce optimal brood sizes than ‘reactive’ individuals who have more precise local environmental knowledge. To test this, we quantified exploratory behaviour (a proxy for proactivity) in a great tit (Parus major) population, manipulated brood sizes (reduced, control, enlarged) and evaluated whether individuals of dissimilar coping style differed in their level of optimization. If reactive females behaved optimally, any deviation from their original brood size should lower fitness, whereas this should not be the case for proactive females. Reactive females indeed performed best at their natural brood size, whereas proactive females performed best when raising an enlarged brood. These findings imply that proactive females produced sub-optimal brood sizes. We speculate that proactive females might (i) take decisions based on biased perception of their environment, (ii) face energetic constraints in offspring production and/or (iii) be more willing to invest into current reproduction when given the option. Our findings provide experimental evidence for coping style-related differences in optimal reproductive decisions and life-history strategies.

Sources of (co)variation in alternative siring routes available to male great tits (Parus major)

Males of socially monogamous species can increase their siring success via within‐pair and extra‐pair fertilizations. In this study, we focused on the different sources of (co)variation between these siring routes, and asked how each contributes to total siring success. We quantified the fertilization routes to siring success, as well as behaviors that have been hypothesized to affect siring success, over a five‐year period for a wild population of great tits Parus major. We considered siring success and its fertilization routes as “interactive phenotypes” arising from phenotypic contributions of both members of the social pair. We show that siring success is strongly affected by the fecundity of the social (female) partner. We also demonstrate that a strong positive correlation between extra‐pair fertilization success and paternity loss likely constrains the evolution of these two routes. Moreover, we show that more explorative and aggressive males had less extra‐pair fertilizations, whereas more explorative females laid larger clutches. This study thus demonstrates that (co)variation in siring routes is caused by multiple factors not necessarily related to characteristics of males. We thereby highlight the importance of acknowledging the multilevel structure of male fertilization routes when studying the evolution of male mating strategies.

Statistical Quantification of Individual Differences (SQuID): an educational and statistical tool for understanding multilevel phenotypic data in linear mixed models

1. Phenotypic variation exists in and at all levels of biological organization: variation exists among species, among-individuals within-populations, and in the case of l within-populations abile traits, within-individuals. Mixed-effects models represent ideal tools to quantify multilevel measurements of traits and are being increasingly used in evolutionary ecology. Mixed-effects models are relatively complex, and two main issues may be hampering their proper usage: (i) the relatively few educational resources available to teach new users how to implement and interpret them and (ii) the lack of tools to ensure that the statistical parameters of interest are correctly estimated. In this paper, we introduce Statistical Quantification of Individual Differences (SQuID), a simulation-based tool that can be used for research and educational purposes. SQuID creates a virtual world inhabited by subjects whose phenotypes are generated by a user-defined phenotypic equation, which allows easy translation of biological hypotheses into quantifiable parameters. Statistical Quantification of Individual Differences currently models normally distributed traits with linear predictors, but SQuID is subject to further development and will adapt to handle more complex scenarios in the future. The current framework is suitable for performing simulation studies, determining optimal sampling designs for user-specific biological problems and making simulation-based inferences to aid in the interpretation of empirical studies. Statistical Quantification of Individual Differences is also a teaching tool for biologists interested in learning, or teaching others, how to implement and interpret linear mixed-effects models when studying the processes causing phenotypic variation. Interface-based modules allow users to learn about these issues. As research on effects of sampling designs continues, new issues will be implemented in new modules, including nonlinear and non-Gaussian data.

Demographic measures of an individual’s “pace of life”: fecundity rate, lifespan, generation time, or a composite variable?

Comparative analyses have demonstrated the existence of a ”pace-of-life” (POL) continuum of life-history strategies, from fast-reproducing short-lived species to slow-reproducing long-lived species. This idea has been extended to the concept of a ”pace-of-life syndrome” (POLS), an axis of phenotypic covariation among individuals within species, concerning morphological, physiological, behavioral and life-history traits. Several life-history metrics can be used to place species in the fast-slow continuum; here, we asked whether individual variation in POL can also be studied using similar life-history measures. We therefore translated measures commonly used in demographic studies into individual-level estimates. We studied fecundity rate, generation time, lifespan, age at first reproduction, fecundity at first reproduction, and principal component scores integrating these different metrics. Using simulations, we show how demographic stochasticity and individual variation in resources affect the ability to predict an individual’s POL using these individual-level parameters. We found that their accuracy depends on how environmental stochasticity varies with the species’ position on the fast-slow continuum and with the amount of (co)variation in life-history traits caused by individual differences in resources. These results highlight the importance of studying the sources of life-history covariation to determine whether POL explains the covariation between morphological, physiological, and behavioral traits within species. Our simulations also show that quantifying not only among-individual but also among-population patterns of life-history covariation helps in interpreting demographic estimates in the study of POLSs within species.Significance statementIt has been demonstrated that there is a continuum of life-history strategies, from fast-reproducing short-lived species to slow-reproducing long-lived species. This pattern of variation in the tempo of life-history strategies has been named the pace-of-life continuum. Recently, it has been suggested that within a population, variation in pace of life explains differences between individuals in their morphological, behavioral, and physiological traits. This paper provides guidelines on how to quantify the pace of life of individuals using demographic approaches that have been developed to study the pace of life of species.

Does perceived predation risk affect patterns of extra‐pair paternity? A field experiment in a passerine bird

Non-consumptive predator effects have been shown to influence a wide range of behavioural, life history and morphological traits. Extra-pair reproduction is widespread among socially monogamous birds and may incur predation costs. Consequently, altered rates of extra-pair reproduction are expected in circumstances characterized by increased adult perceived predation risk. In addition, extra-pair reproduction is expected to be most affected for birds with phenotypes that generally increase predation risk (such as more active individuals). In two consecutive years, perceived predation risk was manipulated for great tits Parus major breeding in 12 nest-box plots by broadcasting sounds of their main predator (European sparrowhawk Accipiter nisus;six plots). As a control treatment, sounds of a sympatric, avian non-predator species were broadcast (Eurasian blackbird Turdus merula;six plots). Levels of extra-pair paternity did not differ between plots with different predation risk treatments. Males that moved more in a novel environment (more active or faster exploring) tended to have offspring with fewer partners, but this effect did not vary with predation risk treatment. From an adaptive viewpoint, predation costs associated with extra-pair reproduction may be small and may not outweigh the benefits of extra-pair behaviour. Research on a broader range of taxa with different mating strategies is now needed to confirm the generality of our findings.

Circadian rhythms of urinary cortisol levels vary between individuals in wild male chimpanzees: a reaction norm approach

Investigating the repeatability of trait variation between individuals, that is the amount of individual variation in relation to overall phenotypic variation, indicates an upper level of heritability and reveals whether a given trait may be subject to selection. Labile traits are characterized by high levels of flexibility and consequently low trait repeatability is expected. Indeed, research examining glucocorticoid levels in various non-mammal species found low repeatability scores. However, mammals may be different in this respect as (i) differential maternal care early in life has the potential to prime hypothalamic-pituitary-adrenal axis functioning and (ii) allelic variation affecting hypothalamic-pituitary-adrenal axis functioning has been reported. Individuals often differ from each other in average and/or plastic labile trait expression, two aspects that can be described using a reaction norm approach. Both consistent and flexible reaction norm expression has been argued to serve adaptive purposes, depending on the stability and predictability of environmental conditions. Here we investigated both trait and reaction norm repeatability of urinary cortisol levels in wild adult male chimpanzees. To capture the expression of the circadian urinary cortisol rhythm of individual males over time, urine samples were collected throughout the day. In total data of 30 males collected over a period of 8 years were included in the dataset. No male was sampled over the whole 8-year period however. We found minor levels of trait repeatability but considerable reaction norm repeatability. This implies a minor role of genetic or priming factors on cortisol excretion, but reveals that males differ consistently in average urinary cortisol levels and the shape of the circadian urinary cortisol rhythm. Relating these results to fitness parameters will provide answers to questions on the adaptive value of reaction norm repeatability of this labile hormonal trait in the future.