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.     

Body size,but not age-at-maturation or context,affects the expression of predator-induced behavioural plasticity in female green swordtails (Xiphophorus hellerii)

Behavioural plasticity is a form of reversible phenotypic plasticity in which a genotype can express different behavioural phenotypes under different environmental conditions. Though an interest in among-individual differences in behavioural plasticity has flourished in recent decades, few studies have considered the effects of intrinsic factors, such as life-history or morphological traits, in tandem with extrinsic factors, such as presence of conspecifics in different social contexts, on predator-induced behavioural plasticity. Here, we present a study conducted with female green swordtail fishes, Xiphophorus hellerii, designed to assess the effects of age-at-maturation and body size on the expression of predator-induced behavioural plasticity in two social contexts: (a) female-only (two females) and (b) female-and-male (two females and a male). We further examined the extent to which individual expression of behavioural plasticity is consistent across these two social contexts. We found that in the presence of a predator, focal females were more timid in response to the stimulus and more tolerant of the non-focal female, and small females expressed this change from bold/less tolerant to timid/more tolerant to a greater degree than large females, regardless of age-at-maturation. However, individuals were not consistent in the degree or direction of plasticity expressed in the behaviours of interest between the female-only and the female-and-male context. Here, we show that within- and among-individual differences in behavioural expression are common but inconsistent. How intrinsic and extrinsic factors independently or together drive expression of plasticity in antipredator and agonistic behaviours is varied and warrants further study.     

Candidate gene polymorphisms for behavioural adaptations during urbanization in blackbirds

Successful urban colonization by formerly rural species represents an ideal situation in which to study adaptation to novel environments. We address this issue using candidate genes for behavioural traits that are expected to play a role in such colonization events. We identified and genotyped 16 polymorphisms in candidate genes for circadian rhythms, harm avoidance and migratory and exploratory behaviour in 12 paired urban and rural populations of the blackbird Turdus merula across the Western Palaearctic. An exonic microsatellite in the SERT gene, a candidate gene for harm avoidance behaviour, exhibited a highly significant association with habitat type in an analysis conducted across all populations. Genetic divergence at this locus was consistent in 10 of the 12 population pairs; this contrasts with previously reported stochastic genetic divergence between these populations at random markers. Our results indicate that behavioural traits related to harm avoidance and associated with the SERT polymorphism experience selection pressures during most blackbird urbanization events. These events thus appear to be influenced by homogeneous adaptive processes in addition to previously reported demographic founder events.     

Opposite selection on behavioural types by active and passive fishing gears in a simulated guppy Poecilia reticulata fishery

This study assessed whether fishing gear was selective on behavioural traits, such as boldness and activity, and how this was related with a productivity trait, growth. Female guppies Poecilia reticulata were screened for their behaviour on the shy–bold axis and activity, and then tested whether they were captured differently by passive and active fishing gear, here represented by a trap and a trawl. Both gears were selective on boldness; bold individuals were caught faster by the trap, but escaped the trawl more often. Boldness and gear vulnerability showed weak correlations with activity and growth. The results draw attention to the importance of the behavioural dimension of fishing: selective fishing on behavioural traits will change the trait composition of the population, and might eventually affect resilience and fishery productivity.     

Similar recent selection criteria associated with different behavioural effects in two dog breeds

Selection during the last decades has split some established dog breeds into morphologically and behaviourally divergent types. These breed splits are interesting models for behaviour genetics since selection has often been for few and well‐defined behavioural traits. The aim of this study was to explore behavioural differences between selection lines in golden and Labrador retriever, in both of which a split between a common type (pet and conformation) and a field type (hunting) has occurred. We hypothesized that the behavioural profiles of the types would be similar in both breeds. Pedigree data and results from a standardized behavioural test from 902 goldens (698 common and 204 field) and 1672 Labradors (1023 and 649) were analysed. Principal component analysis revealed six behavioural components: curiosity, play interest, chase proneness, social curiosity, social greeting and threat display. Breed and type affected all components, but interestingly there was an interaction between breed and type for most components. For example, in Labradors the common type had higher curiosity than the field type (F_1,1668 = 18.359; P < 0.001), while the opposite was found in goldens (F_1,897 = 65.201; P < 0.001). Heritability estimates showed considerable genetic contributions to the behavioural variations in both breeds, but different heritabilities between the types within breeds was also found, suggesting different selection pressures. In conclusion, in spite of similar genetic origin and similar recent selection criteria, types behave differently in the breeds. This suggests that the genetic architecture related to behaviour differs between the breeds.     

Examining the link between personality and laterality in a feral guppy Poecilia reticulata population

This study examined whether variation in the strength and direction of lateralization in a detour task was linked with variation in three common personality measurements: boldness, activity and sociability, in a population of wild guppies Poecilia reticulata. Additionally, the aim was to determine whether any consistent correlations between these behavioural traits, known as behavioural syndromes, were present in the study population. The results revealed that all three personality traits were highly repeatable over time in both sexes. Evidence of a complex syndrome in the form of a correlation between boldness, sociability and activity was found; however, this relationship was only present in males. Males that were more active in a familiar environment emerged more quickly from shelter into a novel environment and were more social. In general, male P. reticulata were bold, active and antisocial compared to females, with these differences probably a reflection of opposing life‐history strategies. Only a weak link between the strength of cerebral lateralisation and personality was discovered and this was mediated by sex.     

Social behavioural epistemology and the scientific community

The progress of science is influenced substantially by social behaviour of and social interactions within the scientific community. Similar to innovations in primate groups, the social acceptance of an innovation depends not only upon the relevance of the innovation but also on the social dominance and connectedness of the innovator. There are a number of parallels between many well-known phenomena in behavioural evolution and various behavioural traits observed in the scientific community. It would be useful, therefore, to use principles of behavioural evolution as hypotheses to study the social behaviour of the scientific community. I argue in this paper that a systematic study of social behavioural epistemology is likely to boost the progress of science by addressing several prevalent biases and other problems in scientific communication and by facilitating appropriate acceptance/rejection of novel concepts.     

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.     

Not in their genes: Phenotypic flexibility, behavioural traditions and cultural evolution in wild bonnet macaques

Phenotypic flexibility, or the within-genotype, context-dependent, variation in behaviour expressed by single reproductively mature individuals during their lifetimes, often impart a selective advantage to organisms and profoundly influence their survival and reproduction. Another phenomenon apparently not under direct genetic control is behavioural inheritance whereby higher animals are able to acquire information from the behaviour of others by social learning, and, through their own modified behaviour, transmit such information between individuals and across generations. Behavioural information transfer of this nature thus represents another form of inheritance that operates in many animals in tandem with the more basic genetic system. This paper examines the impact that phenotypic flexibility, behavioural inheritance and socially transmitted cultural traditions may have in shaping the structure and dynamics of a primate society — that of the bonnet macaque (Macaca radiata), a primate species endemic to peninsular India. Three principal issues are considered: the role of phenotypic flexibility in shaping social behaviour, the occurrence of individual behavioural traits leading to the establishment of social traditions, and the appearance of cultural evolution amidst such social traditions. Although more prolonged observations are required, these initial findings suggest that phenotypic plasticity, behavioural inheritance and cultural traditions may be much more widespread among primates than have previously been assumed but may have escaped attention due to a preoccupation with genetic inheritance in zoological thinking. This paper is dedicated with admiration and gratitude to the late Dr Raja Ramanna, a man who held all primates in great esteem.     

Rapid changes in genetic architecture of behavioural syndromes following colonization of a novel environment

Behavioural syndromes, that is correlated behaviours, may be a result from adaptive correlational selection, but in a new environmental setting, the trait correlation might act as an evolutionary constraint. However, knowledge about the quantitative genetic basis of behavioural syndromes, and the stability and evolvability of genetic correlations under different ecological conditions, is limited. We investigated the quantitative genetic basis of correlated behaviours in the freshwater isopod Asellus aquaticus. In some Swedish lakes, A. aquaticus has recently colonized a novel habitat and diverged into two ecotypes, presumably due to habitat‐specific selection from predation. Using a common garden approach and animal model analyses, we estimated quantitative genetic parameters for behavioural traits and compared the genetic architecture between the ecotypes. We report that the genetic covariance structure of the behavioural traits has been altered in the novel ecotype, demonstrating divergence in behavioural correlations. Thus, our study confirms that genetic correlations behind behaviours can change rapidly in response to novel selective environments.     

Host plant effects on the behavioural phenotype of a Chrysomelid

1. The food plant quality influences feeding preferences and various life history traits of herbivorous insects. However, the effects of different host plant qualities on the behavioural phenotype have rarely been studied in behavioural ecology, especially in a pest‐crop‐framework. 2. Behavioural phenotypes of insects may not only be affected by external environmental factors, such as the host plant quality but are also shaped by internal factors, such as the sex and the age of individuals. 3. To study host plant effects on behavioural phenotypes, we reared mustard leaf beetles (Phaedon cochleariae Fabricius) either on their natural host watercress or on the crop cabbage, on which this beetle can be a pest. The behavioural phenotype was characterised twice in the adult lifetime by measuring six behavioural traits tested in distinct contexts. 4. Depending on the context, different behavioural traits were specifically affected by the host plant, the sex and/or the age. Beetles fed on cabbage became more active with age. Furthermore, the boldness tested in an unprotected environment context was influenced by the host, with beetles fed on cabbage being bolder, whereas the boldness in a hiding or predator attack context was affected by the age and/or the interaction of host plant × sex. 5. In conclusion, beetles fed on the crop cabbage develop a different behavioural phenotype compared to beetles fed on watercress. Previous results showed that beetles reared on cabbage have a higher reproductive output. Thus, beetles fed on the crop potentially express a faster pace‐of‐life.     

Personality over ontogeny in zebra finches: long-term repeatable traits but unstable behavioural syndromes

A crucial assumption of animal personality research is that behaviour is consistent over time, showing a high repeatability within individuals. This assumption is often made, sometimes tested using short time intervals between behavioural tests, but rarely thoroughly investigated across long time intervals crossing different stages of ontogeny. We performed such a longitudinal test across three life stages in zebra finches (Taeniopygia guttata), representing about 15-20% of their life span in captivity, and found repeatabilities ranging from 0.03 to 0.67. Fearlessness and exploration were the most repeatable traits both within and across life stages. Activity and aggression were repeatable across, but not or only partly within life stages. Boldness was not repeatable. Furthermore, we found no evidence for a consistent behavioural syndrome structure across ontogeny. Our results indicate that the consistency of behavioural traits and their correlations might be overestimated and suggest that life-long stability of animal personality should not simply be assumed.     

Genetics of behavioural adaptation of livestock to farming conditions

Behavioural adaptation of farm animals to environmental changes contributes to high levels of production under a wide range of farming conditions, from highly controlled indoor systems to harsh outdoor systems. The genetic variation in livestock behaviour is considerable. Animals and genotypes with a larger behavioural capacity for adaptation may cope more readily with varying farming conditions than those with a lower capacity for adaptation. This capacity should be exploited when the aim is to use a limited number of species extensively across the world. The genetics of behavioural traits is understood to some extent, but it is seldom accounted for in breeding programmes. This review summarizes the estimates of genetic parameters for behavioural traits in cattle, pigs, poultry and fish. On the basis of the major studies performed in the last two decades, we focus the review on traits of common interest in the four species. These concern the behavioural responses to both acute and chronic stressors in the physical environment (feed, temperature, etc.) and those in the social environment (other group members, progeny, humans). The genetic strategies used to improve the behavioural capacity for adaptation of animals differ between species. There is a greater emphasis on responses to acute environmental stress in fish and birds, and on responses to chronic social stress in mammals.     

Population differentiation and behavioural association of the two ‘personality’ genes DRD4 and SERT in dunnocks (Prunella modularis)

Quantifying the variation in behaviour‐related genes within and between populations provides insight into how evolutionary processes shape consistent behavioural traits (i.e. personality). Deliberate introductions of non‐native species offer opportunities to investigate how such genes differ between native and introduced populations and how polymorphisms in the genes are related to variation in behaviour. Here, we compared the genetic variation of the two ‘personality’ genes, DRD4 and SERT, between a native (United Kingdom, UK) and an introduced (New Zealand, NZ) population of dunnocks, Prunella modularis. The NZ population showed a significantly lower number of single nucleotide polymorphisms (SNPs) compared to the UK population. Standardized F’_st estimates of the personality genes and neutral microsatellites indicate that selection (anthropogenic and natural) probably occurred during and post the introduction event. Notably, the largest genetic differentiation was found in the intronic regions of the genes. In the NZ population, we also examined the association between polymorphisms in DRD4 and SERT and two highly repeatable behavioural traits: flight‐initiation distance and mating status (promiscuous females and cobreeding males). We found 38 significant associations (for different allele effect models) between the two behavioural traits and the studied genes. Further, 22 of the tested associations showed antagonistic allele effects for males and females. Our findings illustrate how introduction events and accompanying ecological changes could influence the genetic diversity of behaviour‐related genes.     

Personality traits and behavioural profiles in the domestic canary are affected by sex and photoperiod

Personality traits and behavioural profiles are generally assumed to be stable in adulthood. Yet, it has been hypothesised that animals should cope with cyclical fluctuations by adjusting both single behaviours and suites of behaviour. Photoperiod is well known to induce hormonal and physiological changes, and these changes can in turn affect personality traits and behavioural profiles. This study is the first to explicitly investigate the influence of photoperiod on both behavioural profiles and personality traits. Six potential personality traits (within‐flock activity, ability to escape, response to threat, isolation calling, boldness and neophobia) and dominance were measured four times in 96 domestic canaries Serinus canaria (48 males and 48 females): twice during a long photoperiod (Long Days) and 6 months later twice during a short photoperiod (Short Days). Without regard to sex and photoperiod, most traits were highly repeatable, and bolder canaries were more dominant, less sensitive to an external threat and to isolation and less neophobic. In addition, the more active individuals within a flock were the more difficult to catch. Yet, both sex and photoperiod affected personality traits and behavioural profiles. Personality traits remained repeatable within each photoperiod though we observed behavioural plasticity and sex differences for response to threat, neophobia and within‐flock activity. Concerning behavioural profiles, the negative relationship between boldness and neophobia remained homogenous in both sexes during Short Days as well as during Long Days. Then, the more active individuals within a flock were the more difficult to catch in Short Days but not in Long Days. Finally, the other correlations not only varied with photoperiod but also with sex. Our study highlights the importance of photoperiod and sex in the expression of personality traits and behavioural profiles, and of the need to measure them across the whole photoperiodic cycle.     

Lifetime low behavioural plasticity of personality traits in the common vole (Microtus arvalis) under laboratory conditions

Individual differences in behaviour, referred to as animal personality, are consistent across time and contexts. Nevertheless, personality traits show behavioural plasticity, much like many other phenotypic traits. In the present study, we examined the relationship between personality traits and behavioural plasticity in the common vole (Microtus arvalis) under stable, long-lasting laboratory conditions. A total of 94 voles were tested in the classic open field test, designed to measure seven behavioural parameters (distance moved, grooming, immobility, rearing, running, scanning and walking duration) during a three-minute test. A total of 60 voles formed the experimental group and were tested at four different time points over their lifetime (1st, 3rd, 5th and 7th month); 34 voles formed the control group and were tested only once at the 7th month. All voles were of the same age. Based on principal component analysis (PCA), two ordination axes were determined: “exploration” and “activity.” For further analyses, “distance moved” and “scanning duration” were selected from the first axis and “walking duration” from the second. Using linear mixed-effect models (LMMs), we found highly significant random intercepts (i.e. personality traits) in all three behavioural parameters. However, evidence for behavioural plasticity was only found in the distance moved parameter, as determined from the random slope, and correlations between personality trait (intercept) and plasticity (slope) were not significant for any trait. During the experiment, variances of random effects were high and remained essentially the same, whilst the rank order of many individuals changed. Based on fixed effect slopes and a comparison with the control group, habituation was only significant for “walking duration.” The observed low behavioural plasticity could mirror stable (laboratory) conditions that result in the manifestation of original trait settings (genetic, early postnatal) or their gradual overcoming. These findings provide a starting point for further tests on free-living voles.     

X inactivation as a source of behavioural differences in monozygotic female twins.

Although members of monozygotic twin pairs are identical in genome sequence, they may differ in patterns of gene expression. One early and irreversible process affecting gene expression, which can create differences within pairs of female monozygotic twins, is X inactivation - one twin can express mainly paternally-received genes on the X chromosome while the other twin expresses mainly maternally-received genes. It follows that non-identical X chromosome expression may cause female monozygotic twins to correlate less strongly than male monozygotic twins on complex behavioural traits affected by X-linked loci. We tested this hypothesis using data from around 4000 same-sex twin pairs on 9 social, behavioural and cognitive measures at ages 2, 3 and 4. Consistent with our hypothesis, monozygotic males were generally more similar than monozygotic females. Three of four significant differences were in traits showing higher correlations in males than females, and these traits - prosocial behaviour, peer problems, and verbal ability - have all been proposed previously in the literature as being influenced by genes on the X chromosome. Interestingly, dizygotic twins showed the reverse pattern of correlations for similar variables, which is also consistent with the X inactivation hypothesis; taken together, then, our monozygotic and dizygotic results suggest the presence of quantitative trait loci on the X chromosome.     

Personality Predicts Social Dominance in Male Domestic Fowl

Individuals in social species commonly form dominance relationships, where dominant individuals enjoy greater access to resources compared to subordinates. A range of factors such as sex, age, body size and prior experiences has to varying degrees been observed to affect the social status an individual obtains. Recent work on animal personality (i.e. consistent variation in behavioural responses of individuals) demonstrates that personality can co-vary with social status, suggesting that also behavioural variation can play an important role in establishment of status. We investigated whether personality could predict the outcome of duels between pairs of morphologically matched male domestic fowl (Gallus gallus domesticus), a species where individuals readily form social hierarchies. We found that males that more quickly explored a novel arena, or remained vigilant for a longer period following the playback of a warning call were more likely to obtain a dominant position. These traits were uncorrelated to each other and were also uncorrelated to aggression during the initial part of the dominance-determining duel. Our results indicate that several behavioural traits independently play a role in the establishment of social status, which in turn can have implications for the reproductive success of different personality types.     

Male behavioural maturation rate responds to selection on pollen hoarding in honeybees

Division of labour in social insect colonies relies on behavioural functional differentiation (specialization) of individuals with similar genomes. However, individual behavioural traits do not evolve independently of each other (behavioural syndromes). A prime example is the suite of behavioural differences in honeybee workers that has evolved in response to bidirectional selection on pollen hoarding of honeybee colonies (pollen-hoarding syndrome). More generally, these differences reflect functional differentiation between nectar and pollen foragers. We demonstrate here that this pollen-hoarding syndrome extends to drones. Similar to what has been shown in workers, drones from the high-pollen-hoarding strain had a higher locomotion activity after emergence, and they initiated flight earlier than did males derived from the low-pollen-hoarding strain, with hybrids intermediate. However, these two behavioural traits were unlinked at the individual level. We also found that social environment (the colony) affects the age at which drones initiate flight. The indirect selection responses of male behaviour suggest that male and worker evolution are not independent and may constrain each other's evolution. Furthermore, we identified three distinct peaks in the probability of flight initiation over the course of the experiment and a decreased phenotypic variability in the 'hybrid' males, contrary to quantitative genetic expectations.     

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.