Social inheritance of avoidances shapes the structure of animal social networks.

Social structure can have significant effects on selection, affecting both individual fitness traits and population-level processes. As such, research into its dynamics and evolution has spiked in the last decade, where theoretical and computational advances in social network analysis have increased our understanding of its ecological and inheritance underpinnings. Yet, the processes that shape the formation of structure within social networks are poorly understood and the role of social avoidances unknown. Social avoidances are an alternate of social affiliation in animal societies, which, although invisible, likely play a role in shaping animal social networks. Assuming social avoidances evolve under similar constraints as affiliative behavior, we extended a previous model of social inheritance of affiliations to investigate the impact of social inheritance of avoidances on social network structure. We modeled avoidances as relationships that individuals can copy from their mothers or from their mother's social environment and varied the degrees to which individuals inherit social affiliates and avoidances to test their combined influence on social network structure. We found that inheriting avoidances via maternal social environments made social networks less dense and more modular, thereby demonstrating how social avoidance can shape the evolution of animal social networks.

Selection in the city: Rapid and fine-scale evolution of urban eastern water dragons.

Oceanic archipelagos have long been treated as a Petri dish for studies of evolutionary and ecological processes. Like archipelagos, cities exhibit similar patterns and processes, such as the rapid phenotypic divergence of a species between urban and nonurban environments. However, on a local scale, cities can be highly heterogenous, where geographically close populations can experience dramatically different environmental conditions. Nevertheless, we are yet to understand the evolutionary and ecological implications for populations spread across a heterogenous cityscape. To address this, we compared neutral genetic divergence to quantitative trait divergence within three native riparian and four city park populations of an iconic urban adapter, the eastern water dragon. We demonstrated that selection is likely acting to drive divergence of snout-vent length and jaw width across native riparian populations that are geographically isolated and across city park populations that are geographically close yet isolated by urbanization. City park populations as close as 0.9 km exhibited signs of selection-driven divergence to the same extent as native riparian populations isolated by up to 114.5 km. These findings suggest that local adaptation may be occurring over exceptionally small geographic and temporal scales within a single metropolis, demonstrating that city parks can act as archipelagos for the study of rapid evolution.

A variance partitioning perspective of assortative mating: Proximate mechanisms and evolutionary implications.

Assortative mating occurs when paired individuals of the same population are more similar than expected by chance. This form of non-random assortment has long been predicted to play a role in many evolutionary processes because assortatively mated individuals are assumed to be genetically similar. However, this assumption may always hold for labile traits, or traits that are measured with error. For such traits, there is a variety of proximate mechanisms that can drive phenotypic resemblance between mated partners that, notably, have very different evolutionary repercussions. Bettering our understanding of the role of assortative mating in evolution will thus require insight into its proximate causes. To date, empirical research remains sparse, especially when for labile traits. This special issue aims to stimulate such research while promoting the usage and development of statistical approaches allowing the quantification of the relative roles of alternative proximate mechanisms causing assortative mating. To this end, we first describe how the phenotypic covariance between mated partners can be usefully partitioned into components that capture one or several of five distinct mechanisms. We then demonstrate why the importance of mechanisms causing genetic covariance between the traits of partners may often be overestimated. Finally, we detail how the evolutionary causes and consequences of the diverse mechanisms may be identified.

Estimating the long-term repeatability of food-hoarding behaviours in an avian predator.

Food-hoarding behaviour is widespread in the animal kingdom and enables predictable access to food resources in unpredictable environments. Within species, consistent variation among individuals in food-hoarding behaviours may indicate the existence of individual strategies, as it likely captures intrinsic differences in how individuals cope with risks (e.g. starvation, pilferage). Using 17 years of data, we estimated the long-term repeatability of 10 food-hoarding behaviours in a population of Eurasian pygmy owls (Glaucidium passerinum), a small avian predator subject to high temporal fluctuations in its main prey abundance. We found low repeatability in the proportion of shrews and the average prey mass stored for both sexes, while females were moderately repeatable in the mass and the number of prey items stored. These two pairs of behaviours were tightly correlated among individuals and might represent two different sets of individual strategies to buffer against starvation risks.

Collision between biological process and statistical analysis revealed by mean centring.

Animal ecologists often collect hierarchically structured data and analyse these with linear mixed-effects models. Specific complications arise when the effect sizes of covariates vary on multiple levels (e.g. within vs. among subjects). Mean centring of covariates within subjects offers a useful approach in such situations, but is not without problems. A statistical model represents a hypothesis about the underlying biological process. Mean centring within clusters assumes that the lower level responses (e.g. within subjects) depend on the deviation from the subject mean (relative) rather than on the absolute scale of the covariate. This may or may not be biologically realistic. We show that mismatch between the nature of the generating (i.e. biological) process and the form of the statistical analysis produce major conceptual and operational challenges for empiricists. We explored the consequences of mismatches by simulating data with three response-generating processes differing in the source of correlation between a covariate and the response. These data were then analysed by three different analysis equations. We asked how robustly different analysis equations estimate key parameters of interest and under which circumstances biases arise. Mismatches between generating and analytical equations created several intractable problems for estimating key parameters. The most widely misestimated parameter was the among-subject variance in response. We found that no single analysis equation was robust in estimating all parameters generated by all equations. Importantly, even when response-generating and analysis equations matched mathematically, bias in some parameters arose when sampling across the range of the covariate was limited. Our results have general implications for how we collect and analyse data. They also remind us more generally that conclusions from statistical analysis of data are conditional on a hypothesis, sometimes implicit, for the process(es) that generated the attributes we measure. We discuss strategies for real data analysis in face of uncertainty about the underlying biological process.

Can dominance genetic variance be ignored in evolutionary quantitative genetic analyses of wild populations?

Accurately estimating genetic variance components is important for studying evolution in the wild. Empirical work on domesticated and wild outbred populations suggests that dominance genetic variance represents a substantial part of genetic variance, and theoretical work predicts that ignoring dominance can inflate estimates of additive genetic variance. Whether this issue is pervasive in natural systems is unknown, because we lack estimates of dominance variance in wild populations obtained in situ. Here, we estimate dominance and additive genetic variance, maternal variance, and other sources of nongenetic variance in eight traits measured in over 9000 wild nestlings linked through a genetically resolved pedigree. We find that dominance variance, when estimable, does not statistically differ from zero and represents a modest amount (2-36%) of genetic variance. Simulations show that (1) inferences of all variance components for an average trait are unbiased; (2) the power to detect dominance variance is low; (3) ignoring dominance can mildly inflate additive genetic variance and heritability estimates but such inflation becomes substantial when maternal effects are also ignored. These findings hence suggest that dominance is a small source of phenotypic variance in the wild and highlight the importance of proper model construction for accurately estimating evolutionary potential.

Exploratory behavior undergoes genotype-age interactions in a wild bird.

Animal personality traits are often heritable and plastic at the same time. Indeed, behaviors that reflect an individual's personality can respond to environmental factors or change with age. To date, little is known regarding personality changes during a wild animals' lifetime and even less about stability in heritability of behavior across ages. In this study, we investigated age-related changes in the mean and in the additive genetic variance of exploratory behavior, a commonly used measure of animal personality, in a wild population of great tits. Heritability of exploration is reduced in adults compared to juveniles, with a low genetic correlation across these age classes. A random regression animal model confirmed the occurrence of genotype-age interactions (G×A) in exploration, causing a decrease in additive genetic variance before individuals become 1 year old, and a decline in cross-age genetic correlations between young and increasingly old individuals. Of the few studies investigating G×A in behaviors, this study provides rare evidence for this phenomenon in an extensively studied behavior. We indeed demonstrate that heritability and cross-age genetic correlations in this behavior are not stable over an individual's lifetime, which can affect its potential response to selection. Because G×A is likely to be common in behaviors and have consequences for our understanding of the evolution of animal personality, more attention should be turned to this phenomenon in the future work.

Tail colour signals performance in blue tit nestlings.

Indirect sexual selection arises when reproductive individuals choose their mates based on heritable ornaments that are genetically correlated to fitness. Evidence for genetic associations between ornamental colouration and fitness remains scarce. In this study, we investigate the quantitative genetic relationship between different aspects of tail structural colouration (brightness, hue and UV chroma) and performance (cell-mediated immunity, body mass and wing length) in blue tit (Cyanistes caeruleus) nestlings. In line with previous studies, we find low heritability for structural colouration and moderate heritability for performance measures. Multivariate animal models show positive genetic correlations between the three measures of performance, indicating quantitative genetic variation for overall performance, and tail brightness and UV chroma, two genetically independent colour measures, are genetically correlated with performance (positively and negatively, respectively). Our results suggest that mate choice based on independent aspects of tail colouration can have fitness payoffs in blue tits and provide support for the indirect benefits hypothesis. However, low heritability of tail structural colouration implies that indirect sexual selection on mate choice for this ornament will be a weak evolutionary force.

Shared environmental effects bias phenotypic estimates of assortative mating in a wild bird.

Assortative mating is pervasive in wild populations and commonly described as a positive correlation between the phenotypes of males and females across mated pairs. This correlation is often assumed to reflect non-random mate choice based on phenotypic similarity. However, phenotypic resemblance between mates can also arise when their traits respond plastically to a shared environmental effect creating a (within-pair) residual correlation in traits. Using long-term data collected in pairs of wild blue tits and a covariance partitioning approach, we empirically demonstrate that such residual covariance indeed exists and can generate phenotypic correlations (or mask assortative mating) in behavioural and morphometric traits. These findings (i) imply that residual covariance is likely to be common and bias phenotypic estimates of assortative mating, which can have consequences for evolutionary predictions, (ii) call for the use of rigorous statistical approaches in the study of assortative mating, and (iii) show the applicability of one of these approaches in a common study system.

A strong genetic correlation underlying a behavioural syndrome disappears during development because of genotype-age interactions.

In animal populations, as in humans, behavioural differences between individuals that are consistent over time and across contexts are considered to reflect personality, and suites of correlated behaviours expressed by individuals are known as behavioural syndromes. Lifelong stability of behavioural syndromes is often assumed, either implicitly or explicitly. Here, we use a quantitative genetic approach to study the developmental stability of a behavioural syndrome in a wild population of blue tits. We find that a behavioural syndrome formed by a strong genetic correlation of two personality traits in nestlings disappears in adults, and we demonstrate that genotype-age interaction is the likely mechanism underlying this change during development. A behavioural syndrome may hence change during organismal development, even when personality traits seem to be strongly physiologically or functionally linked in one age group. We outline how such developmental plasticity has important ramifications for understanding the mechanistic basis as well as the evolutionary consequences of behavioural syndromes.

The importance of genotype-by-age interactions for the development of repeatable behavior and correlated behaviors over lifetime.

Behaviors are highly plastic and one aspect of this plasticity is behavioral changes over age. The presence of age-related plasticity in behavior opens up the possibility of between-individual variation in age-related plasticity (Individual-Age interaction, IxA) and genotype-age interaction (GxA). We outline the available approaches for quantifying GxA. We underline that knowledge of GxA for behaviors is an important step in reaching and understanding of the evolution of plasticity in behavior over lifetime. In particular, the heritability (repeatability) and/or the rank order of behavior across individuals are predicted to change across ages in presence of GxA. We draw on the theory of reaction norms to illustrate that GxA, when present, is likely to lead to developmental changes in the magnitude and possibly sign of the genetic correlation between behaviors (behavioral syndrome). We present an overview of the literature on changes in the ranking of individuals' behavior across ages, and in the correlation between behaviors. Although all studies were carried out on the phenotypic level, they overall suggest clear scope for increased study of GxA as a process explaining age-related plasticity in behaviors. Lastly, we throughout emphasize that many of the approaches and underlying theory of GxA is applicable to the study of IxA, which is informative as it presents the upper limit of GxA, but is also a more attainable target of study in many systems. Empirical work aimed at understanding IxA and GxA in behavior is needed in order to understand whether patterns predicted by theory on plasticity indeed occur for age-related plasticity of behavior.

Evolutionary quantitative genetics of behavioral responses to handling in a wild passerine.

Behavioral differences between individuals that are consistent over time characterize animal personality. The existence of such consistency contrasts to the expectation based on classical behavioral theory that facultative behavior maximizes individual fitness. Here, we study two personality traits (aggression and breath rate during handling) in a wild population of blue tits during 2007-2012. Handling aggression and breath rate were moderately heritable (h (2) = 0.35 and 0.20, respectively) and not genetically correlated (r A = 0.06) in adult blue tits, which permits them to evolve independently. Reciprocal cross-fostering (2007-2010) showed that offspring reared by more aggressive males have a higher probability to recruit. In addition, offspring reared by pairs mated assortatively for handling aggression had a higher recruitment probability, which is the first evidence that both parents' personalities influence their reproductive success in the wild in a manner independent of their genetic effects. Handling aggression was not subjected to survival selection in either sex, but slow-breathing females had a higher annual probability of survival as revealed by capture-mark-recapture analysis. We find no evidence for temporal fluctuations in selection, and thus conclude that directional selection (via different fitness components) acts on these two heritable personality traits. Our findings show that blue tit personality has predictable fitness consequences, but that facultative adjustment of an individual's personality to match the fitness maximum is likely constrained by the genetic architecture of personality. In the face of directional selection, the presence of heritable variation in personality suggests the existence of a trade-off that we have not identified yet.

Different risk thresholds in pedestrian road crossing behaviour: a comparison of French and Japanese approaches.

When crossing the road, pedestrians have to make a trade-off between saving time and avoiding any risk of injuries. Here, we studied how culture influences an individual's perception of risks when crossing a street, using survival analysis. This study is the first to use this analysis to assess cognitive mechanisms and optimality of decisions underlying road crossing behaviour. We observed pedestrian behaviour in two city centres: Inuyama (Japan) and Strasbourg (France). In each city, observations were made at a safe site consisting of a crosswalk and a street light and at an unsafe site (i.e. no crosswalk or street light). At the unsafe site, we measured the time needed by a pedestrian to take a decision (Tdec). During Tdec, a pedestrian estimates whether he can (Tsafe) or cannot (Trisk) cross the road. Using survival analysis, we studied the distributions of these three time variables and showed that French pedestrians took more risks than Japanese pedestrians, and that males took more risks than females, but only in Japan. More studies would considerably broaden our understanding on how culture may affect decision-making processes under risky circumstances.