Sex and the Syndrome: Individual and Population Consistency in Behaviour in Rock Pool Prawn Palaemon elegans

Animal personality has been widely documented across a range of species. The concept of personality is composed of individual behavioural consistency across time and between situations, and also behavioural trait correlations known as behavioural syndromes. Whilst many studies have now investigated the stability of individual personality traits, few have analysed the stability over time of entire behavioural syndromes. Here we present data from a behavioural study of rock pool prawns. We show that prawns are temporally consistent in a range of behaviours, including activity, exploration and boldness, and also that a behavioural syndrome is evident in this population. We find correlations between many behavioural traits (activity, boldness, shoaling and exploration). In addition, behavioural syndrome structure was consistent over time. Finally, few studies have explicitly studied the role of sex differences in personality traits, behavioural consistency and syndrome structure. We report behavioural differences between male and female prawns but no differences in patterns of consistency. Our study adds to the growing literature on animal personality, and provides evidence showing that syndromes themselves can exhibit temporal consistency.     

Heritability and genetic correlations of personality traits in a wild population of yellow‐bellied marmots (Marmota flaviventris)

Describing and quantifying animal personality is now an integral part of behavioural studies because individually distinctive behaviours have ecological and evolutionary consequences. Yet, to fully understand how personality traits may respond to selection, one must understand the underlying heritability and genetic correlations between traits. Previous studies have reported a moderate degree of heritability of personality traits, but few of these studies have either been conducted in the wild or estimated the genetic correlations between personality traits. Estimating the additive genetic variance and covariance in the wild is crucial to understand the evolutionary potential of behavioural traits. Enhanced environmental variation could reduce heritability and genetic correlations, thus leading to different evolutionary predictions. We estimated the additive genetic variance and covariance of docility in the trap, sociability (mirror image stimulation), and exploration and activity in two different contexts (open‐field and mirror image simulation experiments) in a wild population of yellow‐bellied marmots (Marmota flaviventris). We estimated both heritability of behaviours and of personality traits and found nonzero additive genetic variance in these traits. We also found nonzero maternal, permanent environment and year effects. Finally, we found four phenotypic correlations between traits, and one positive genetic correlation between activity in the open‐field test and sociability. We also found permanent environment correlations between activity in both tests and docility and exploration in the MIS test. This is one of a handful of studies to adopt a quantitative genetic approach to explain variation in personality traits in the wild and, thus, provides important insights into the potential variance available for selection.     

Innovation as part of a wider behavioural syndrome in the guppy: The effect of sex and body size

Recent work on animal personalities has shown that individuals within populations often differ consistently in various types of behaviour and that many of these behaviours correlate among individuals to form behavioural syndromes. Individuals of certain species have also been shown to differ in their rate of behavioural innovation in arriving at novel solutions to new and existing problems (e.g., mazes, novel foods). Here, we investigate whether behaviours traditionally studied in personality research are correlated with individual rates of innovation as part of a wider behavioural syndrome. Guppies (Poecilia reticulata) of both sexes from three different wild population sources were assessed: (a) exploration of an open area; (b) speed through a three‐dimensional maze; (c) investigation of a novel object; and (d) attraction to a novel food. The covariance structure (syndrome structure) was examined using structural equation modelling. The best model separated behaviours relating to activity in all contexts from rates of exploration/investigation and innovation. Innovative behaviour (utilizing new food and moving through a novel area) in these fish therefore forms part of the same syndrome as the traditional shy‐bold continuum (exploration of an open area and investigation of a novel object) found in many animal personality studies. There were no clear differences in innovation or syndrome structure between the sexes, or between the three different populations. However, body size was implicated as part of the behavioural syndrome structure, and because body size is highly correlated with age in guppies, this suggests that individual behavioural differences in personality/innovation in guppies may largely be driven by developmental state.     

Unravelling the Philosophies Underlying ‘Animal Personality’ Studies: A Brief Re‐Appraisal of the Field

The last decade has seen lots of studies on ‘animal personality’ (i.e. the study of consistent between‐individual behavioural differences). As timely and promising as this field is, its development has come with a diversity of research questions. As an unfortunate consequence, it now suffers from substantial confusion about what ‘animal personality’ is, and how relevant related research frameworks are. Here, we stress the current inconsistencies and sources of confusion pertaining to the field, and their consequences on terminology used and miscommunication between researchers. In an attempt to unravel and clarify the concepts underlying the field, we identify two distinct, but complementary, theory‐driven conceptual frameworks: the intra‐individual variability (IIV) approach and the life‐history (LH) approach, which we believe encompass the vast majority of existing ‘personality studies’. Finally, we argue in favour of theory‐driven studies of consistent behavioural differences and state that the integrative statistical properties of random regression models should not override the merit of alternative conceptual frameworks. We then provide brief guidelines and warnings for a parsimonious and sound use of terminology.     

Validating standardised personality tests under semi‐natural conditions in wild house mice (Mus musculus domesticus)

Personality traits in animals are often measured using standardised behavioural tests for activity, boldness/shyness, sociability, aggression and exploration. These tests are quick and convenient, as well as easy to repeat. As the interest in studying the impact of animal personality on ecological and evolutionary consequences has been growing rapidly, there is increasing focus on cross‐validating measurements taken during these tests with behaviours shown under natural situations. In our experiment, we aimed to study the relationship between standardised measurements for activity, exploration and anxiety‐like behaviour measured in Open Field, Novel Object and Elevated Plus Maze tests with exploration and colonisation in semi‐natural conditions. We carried out a semi‐natural enclosure experiment in parallel with standardised behavioural tests, creating a scenario similar to an invasion or dispersal event. We compared behaviours in standardised tests and in enclosures for animals of two populations of wild house mice (Mus musculus domesticus). Several behavioural variables taken during the standardised tests, such as distance moved and time spent with novel object, were negatively correlated with space‐use in the enclosure while being highly positively correlated among each other. Based on their relationship with space use, we refer to behavioural measurements from standardised tests as activity/exploration. The time spent near the walls in an open field, probably reflecting anxiety, was not correlated to any other variable or the behaviour in the enclosure. In addition, we found differences in activity/exploration behaviour between the two populations in the standardised tests, but not during the colonisation of the novel environment. These results emphasise that researchers have to be careful when trying to extrapolate behaviour shown in standardised laboratory test setups to more natural, ecologically relevant situations. This has to be taken into account in distantly related species but even when studying the wild relative of laboratory rodents, for which these standardised tests have originally been developed.     

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

Understanding how animal personality (consistent between‐individual behavioural differences) arises has become a central topic in behavioural sciences. This endeavour is complicated by the fact that not only the mean behaviour of individuals (behavioural type) but also the strength of their reaction to environmental change (behavioural plasticity) varies consistently. Personality and cognitive abilities are linked, and we suggest that behavioural plasticity could also be explained by differences in brain size (a proxy for cognitive abilities), since accurate decisions are likely essential to make behavioural plasticity beneficial. We test this idea in guppies (Poecilia reticulata), artificially selected for large and small brain size, which show clear cognitive differences between selection lines. To test whether those lines differed in behavioural plasticity, we reared them in groups in structurally enriched environments and then placed adults individually into empty tanks, where we presented them daily with visual predator cues and monitored their behaviour for 20 days with video‐aided motion tracking. We found that individuals differed consistently in activity and risk‐taking, as well as in behavioural plasticity. In activity, only the large‐brained lines demonstrated habituation (increased activity) to the new environment, whereas in risk‐taking, we found sensitization (decreased risk‐taking) in both brain size lines. We conclude that brain size, potentially via increasing cognitive abilities, may increase behavioural plasticity, which in turn can improve habituation to novel environments. However, the effects seem to be behaviour‐specific. Our results suggest that brain size likely explains some of the variation in behavioural plasticity found at the intraspecific level.     

Sequential hermaphroditism and personality in a clonal vertebrate: the mangrove killifish

Individuals are regularly documented to consistently differ in their behavioural types (BTs). For example, some individuals are bold whereas others are shy. Within the human personality literature, the big five personality dimensions are commonly documented to be sex-specific with testosterone suggested to underpin traits such as aggressiveness. In non-human animals recent research suggests sex-specific BT expression may be influenced by ecology, mating system and sexual selection. While most research on sex-specific personality has focused on dioecious species, we explore sex differences in BT expression in a sequential hermaphrodite the mangrove killifish. We replicate within 7 isogenic genotypes and investigate sex differences (hermaphrodite and secondary male) in three BTs (exploration, boldness and aggression). This approach allows us to investigate sex differences in BT expression whilst controlling for genetic variation. In this study we find that both secondary males and hermaphrodites are repeatable at the individual level yet there was no difference between the sexes in average BT scores. Furthermore, aggression scores differed between genotypes, and were repeatable at the genotype level, suggesting strong genetic control. Finally, male boldness was significantly more repeatable than hermaphrodites potentially supporting recent proposals relating to sexual selection. We document a behavioural syndrome in male fish with bolder individuals being more aggressive, this behavioural syndrome was not observed however in hermaphrodites. In contrast to a previous developmental study in this species exploration did not correlate with either aggression or boldness in either males or hermaphrodites.     

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.     

Species‐level repertoire size predicts a correlation between individual song elaboration and reproductive success

Birdsong has long been considered a sexually selected trait that relays honest information about male quality, and laboratory studies generally suggest that female songbirds prefer larger repertoires. However, analysis of field studies across species surprisingly revealed a weak correlation between song elaboration and reproductive success, and it remains unknown why only certain species show this correlation in nature. Taken together, these studies suggest that females in numerous species can detect and prefer larger repertoires in a laboratory setting, but larger individual repertoires correlate with reproductive success only in a subset of these species. This prompts the question: Do the species that show a stronger correlation between reproductive success and larger individual repertoires in nature have anything in common? In this study, we test whether between‐species differences in two song‐related variables—species average syllable repertoire size and adult song stability over time—can be used to predict the importance of individual song elaboration in reproductive success within a species. Our cross‐species meta‐analysis of field studies revealed that species with larger average syllable repertoire sizes exhibited a stronger correlation between individual elaboration and reproductive success than species with smaller syllable repertoires. Song stability versus plasticity in adulthood provided little predictive power on its own, suggesting that the putative correlation between repertoire size and age in open‐ended learners does not explain the association between song elaboration and reproductive success.     

Natural selection,plasticity and the emergence of a behavioural syndrome in the wild

Individuals often show consistent behavioural differences where behaviours can form integrated units across functionally different contexts. However, the factors causing and maintaining behavioural syndromes in natural populations remain poorly understood. In this study, we provide evidence for the emergence of a behavioural syndrome during the first months of life in wild brown trout (Salmo trutta). Behavioural traits of trout were scored before and after a 2‐month interval covering a major survival bottleneck, whereupon the consistency and covariance of behaviours were analysed. We found that selection favoured individuals with high activity levels in an open‐field context, a personality trait consistent throughout the duration of the experiment. In addition, a behavioural syndrome emerged over the 2 months in the wild, linking activity to aggressiveness and exploration tendency. These novel results suggest that behavioural syndromes can emerge rapidly in nature from interaction between natural selection and behavioural plasticity affecting single behaviours.     

Heritability and social brood effects on personality in juvenile and adult life‐history stages in a wild passerine

How has evolution led to the variation in behavioural phenotypes (personalities) in a population? Knowledge of whether personality is heritable, and to what degree it is influenced by the social environment, is crucial to understanding its evolutionary significance, yet few estimates are available from natural populations. We tracked three behavioural traits during different life‐history stages in a pedigreed population of wild house sparrows. Using a quantitative genetic approach, we demonstrated heritability in adult exploration, and in nestling activity after accounting for fixed effects, but not in adult boldness. We did not detect maternal effects on any traits, but we did detect a social brood effect on nestling activity. Boldness, exploration and nestling activity in this population did not form a behavioural syndrome, suggesting that selection could act independently on these behavioural traits in this species, although we found no consistent support for phenotypic selection on these traits. Our work shows that repeatable behaviours can vary in their heritability and that social context influences personality traits. Future efforts could separate whether personality traits differ in heritability because they have served specific functional roles in the evolution of the phenotype or because our concept of personality and the stability of behaviour needs to be revised.     

Context is key: A comment on Herczeg et al. 2019

In the last several years, there has been a surge in the number of studies addressing the causes and consequences of among‐individual variation in cognitive ability and behavioural plasticity. Here, we use a recent publication by Herczeg et al. (2019: 32(3), 218–226) to highlight three shortcomings common to this newly emerging field. In their study, Herczeg et al. attempted to link variation in cognitive ability and behavioural plasticity by testing whether selection lines of guppies (Poecilia reticulata) that differ in relative brain size also differ in behavioural plasticity, as might be expected if the costs to plasticity are predominantly derived from the cost of developing large brains. First, residual brain size may not be a suitable proxy for ‘cognitive ability’. Recent work has shown that intraspecific variation in cognitive ability can be better understood by considering variation in the specific brain areas responsible for the relevant behaviours as opposed to whole‐brain mass. Second, the measure of behavioural plasticity, habituation, is unlikely to fulfil the assumptions that plasticity is both adaptive and costly. Finally, we point out several misconceptions regarding animal personality that continue to contribute to the choice of traits that are not well aligned with study objectives. Elucidating the mechanisms underlying among‐individual variation in cognition and behavioural plasticity within populations requires integration between behavioural ecology and comparative cognition, and the study system developed by Herczeg et al. has the potential to provide important mechanistic insights. We hope that by articulating and critically appraising the underlying assumptions that are common in these traditionally separate disciplines, a strong foundation can emerge to allow for more fruitful integration of these fields.     

Linking behavioural syndromes and cognition: a behavioural ecology perspective

With the exception of a few model species, individual differences in cognition remain relatively unstudied in non-human animals. One intriguing possibility is that variation in cognition is functionally related to variation in personality. Here, we review some examples and present hypotheses on relationships between personality (or behavioural syndromes) and individual differences in cognitive style. Our hypotheses are based largely on a connection between fast-slow behavioural types (BTs; e.g. boldness, aggressiveness, exploration tendency) and cognitive speed-accuracy trade-offs. We also discuss connections between BTs, cognition and ecologically important aspects of decision-making, including sampling, impulsivity, risk sensitivity and choosiness. Finally, we introduce the notion of cognition syndromes, and apply ideas from theories on adaptive behavioural syndromes to generate predictions on cognition syndromes.     

Differences in behavioural traits among native and introduced colonies of an invasive ant

Identifying the factors that promote the success of biological invasions is a key pursuit in ecology. To date, the link between animal personality and invasiveness has rarely been studied. Here, we examined in the laboratory how Argentine ant populations from the species’ native and introduced ranges differed in a suite of behaviours related to species interactions and the use of space. We found correlations among specific behavioural traits that defined an explorative-aggressive syndrome. The Main “European” supercolony (introduced range) more readily explored novel environments, displayed more aggression, detected food resources more quickly, and occupied more space than the Catalonian supercolony (introduced range) and two other Argentine supercolonies (native range). The two native supercolonies also differed in their personalities; one harbouring the less invasive personality, while the other is intermediate between the two introduced supercolonies. Therefore, instead of a binary pattern, Argentine ant supercolonies display a behavioural continuum that is independent on their geographic origin (native/introduced ranges). Our results also suggest that variability in personality traits is correlated to differences in the ecological success of Argentine ant colonies. Differences in group personalities may facilitate the persistence and invasion of animals under novel selective pressures by promoting adaptive behaviours. We stress that the concept of animal personality should be taken into account when elucidating the mechanisms of invasiveness.     

Social Dominance in a Gregarious Bird is Related to Body Size But not to Standard Personality Assays

The recent growth of research on animal personality could provide new insights into our understanding of sociality and the structure of animal groups. Although simple assays of the type commonly used to study animal personality have been shown to correlate with social aggressiveness in some bird species, conflicting empirical results do not yet make it clear when such assays, typically using isolated individuals, predict behaviour within social groups. We measured aggressiveness in groups of a very gregarious species, the common waxbill (Estrilda astrild), and performed five commonly used behavioural assays on the same individuals: tonic immobility, mirror test, novel object test, open‐field test and a variant of the latter in an enriched environment. We found that larger individuals were more dominant and that differences in aggressiveness were repeatable. None of the traditional behavioural assays were related to aggressiveness or dominance. Standard personality assays may fail to capture individual differences relevant to predict social behaviour, and we discuss biological and methodological explanations for these results, such as social behaviour being in part an emergent property of groups rather than an intrinsic property of individuals, or gregarious species being particularly sensitive to the conditions of standard personality assays that test individuals alone.     

Behavioural Syndromes in Urban and Rural Populations of Song Sparrows

Animals in urban habitats are often noticeably bold in the presence of humans. Such boldness may arise due to habituation, as urban animals learn, through repeated exposure, that passing humans do not represent a threat. However, there is growing research suggesting that: (1) inherent traits, as opposed to learned behaviour, influence which species invade urban habitats, and (2) individuals exhibit individual personality traits that limit behavioural flexibility, with the possible result that not all individuals would be able to demonstrate an appropriate level of boldness in urban environments. As a result, perhaps only birds with inherently bold personalities could successfully settle in an area of high human disturbance, and further, we might also expect to see the existence of behavioural syndromes, where boldness is correlated with variation in other behavioural traits such as aggression. In this study, we examined boldness and territorial aggression in urban and rural populations of song sparrows. We found that urban birds were bolder towards humans and that urban birds also showed higher levels of territorial aggression. We also found an overall correlation between boldness and territorial aggression, suggesting that urban boldness may be part of a behavioural syndrome. However, we see no correlation between boldness and aggression in the urban population, and thus, more work is needed to determine the mechanisms accounting for high levels of boldness and aggression urban song sparrows.     

Resource availability and plant diversity explain patterns of invasion of an exotic grass

Aims In this study, we examine two common invasion biology hypotheses—biotic resistance and fluctuating resource availability—to explain the patterns of invasion of an invasive grass, Microstegium vimineum.Methods We used 13-year-old deer exclosures in Great Smoky Mountains National Park, USA, to examine how chronic disturbance by deer browsing affects available resources, plant diversity, and invasion in an understory plant community. Using two replicate 1 m 2 plots in each deer browsed and unbrowsed area, we recorded each plant species present, the abundance per species, and the fractional percent cover of vegetation by the cover classes: herbaceous, woody, and graminoid. For each sample plot, we also estimated overstory canopy cover, soil moisture, total soil carbon and nitrogen, and soil pH as a measure of abiotic differences between plots.Important findings We found that plant community composition between chronically browsed and unbrowsed plots differed markedly. Plant diversity was 40% lower in browsed than in unbrowsed plots. At our sites, diversity explained 48% and woody plant cover 35% of the variation in M. vimineum abundance. In addition, we found 3.3 times less M. vimineum in the unbrowsed plots due to higher woody plant cover and plant diversity than in the browsed plots. A parsimonious explanation of these results indicate that disturbances such as herbivory may elicit multiple conditions, namely releasing available resources such as open space, light, and decreasing plant diversity, which may facilitate the proliferation of an invasive species. Finally, by testing two different hypotheses, this study addresses more recent calls to incorporate multiple hypotheses into research attempting to explain plant invasion.     

The Relationship Between Foraging,Learning Abilities and Neophobia in Two Species of Darwin’s Finches

The ability to unlearn a previously established association is an important component of behavioural flexibility and may vary according to species ecology. Previously, two closely related sympatric Darwin’s finches were found to differ in their learning abilities. Small tree finches (Camarhynchus parvulus) outperformed woodpecker finches (Cactospiza pallida) in reversal learning but performed worse in an operant task. We attributed this difference to the habit of woodpecker finches to engage in long bouts of energetic pecking during extractive foraging. Persistently repeating one action without reward could favour performance in operant tasks but also limit behavioural flexibility. Here, we tested whether perseverance is the reason for woodpecker finches’ depressed reversal learning performance. Two new reversal conditions allowed the disentanglement of two sources of error in reversal learning: perseverant choice of the previously rewarded stimulus and failure to respond to the previously non‐rewarded stimulus. For the within‐species comparison, we predicted that woodpecker finches should find it more difficult to learn to avoid the previously rewarded stimulus than learning to choose the previously non‐rewarded stimulus. For the species comparison, we predicted the woodpecker finches should make more errors of perseverance than small tree finches. As performance could also be influenced by reaction to novelty, we compared neophobic responses between species and related them to reversal learning proficiency. We found no significant difference in reversal learning in the predicted direction, but found a negative correlation between neophobia and reversal learning at the inter‐ and the intraspecific level, which points towards a general relationship between reaction to novelty and flexibility.     

Behavioural Phenotypes and the Structure of Human Cognition

Human cognitive uniqueness is often defined in terms of cognitive abilities such as introspection, imitation and cooperativeness. However, little is known about how those traits vary in populations or correlate across individuals. Here we test whether those three cognitive domains are correlated manifestations of an underlying factor, analogous to the psychometric ‘g’ factor, or independent ‘behavioural phenotypes’, analogous to the ‘Big-Five’ personality components. We selected eight variables measuring introspection and extraversion, verbal and physical imitation, cooperation and punishment, and evaluated their individual variability, domain-consistency and sub-structuring in a sample of 84 individuals. Results show high variation and limited clustering into three independent ‘behavioural phenotypes’ of introspection, imitation and cooperation. Only one significant correlation was identified (between two measures of extraversion), while other within-domain measures (introspection vs. extraversion, verbal vs. physical imitation, and cooperation vs. punishment) were not associated. Finally, no between-domain association was identified either through correlations or factor analysis. Overall, the results do not lend support to the hypothesis of a general ‘behavioural phenotype’ underlying individual behaviour. The independence of behaviours of introspection, imitation and cooperation may be the reason why individuals are able to adopt different behavioural strategies (combinations of behavioural phenotypes) and play distinct roles in the maintenance of human distinctive features such as hyper-cooperation and cumulative culture.     

Behaviour‐related DRD4 polymorphisms in invasive bird populations

It has been suggested that individual behavioural traits influence the potential to successfully colonize new areas. Identifying the genetic basis of behavioural variation in invasive species thus represents an important step towards understanding the evolutionary potential of the invader. Here, we sequenced a candidate region for neophilic/neophobic and activity behaviour – the complete exon 3 of the DRD4 gene – in 100 Yellow‐crowned bishops (Euplectes afer) from two invasive populations in Spain and Portugal. The same birds were scored twice for activity behaviour while exposed to novel objects (battery or slice of apple) in captivity. Response to novel objects was repeatable (r = 0.41) within individuals. We identified two synonymous DRD4 SNPs that explained on average between 11% and 15% of the phenotypic variance in both populations, indicating a clear genetic component to the neophilic/neophobic/activity personality axis in this species. This consistently high estimated effect size was mainly due to the repeated measurement design, which excludes part of the within‐individual nongenetic variance in the response to different novel objects. We suggest that the alternative alleles of these SNPs are likely introduced from the original population and maintained by weak or antagonistic selection during different stages of the invasion process. The identified genetic variants have not only the potential to serve as genetic markers of the neophobic/neophilic/activity personality axis, but may also help to understand the evolution of behaviour in these invasive bird populations.