Differences In Behavioral Traits Research Articles

Scientific note on interrupted sexual behavior to virgin queens and expression of male courtship-related gene fruitless in a gynandromorph of bumblebee, Bombus ignitus

Gynandromorphy, which is characterized by the coexistence of male and female tissues in a single individual, is known in insects. Gynandromorphs exhibit diverse levels of defects in sexual behavior. The distribution pattern of both sexes within the nervous systems could be responsible for these differences in behavioral traits; however, most studies have mainly focused on the unique external morphological traits of gynandromorphs, and little attention has been paid to the evaluation of nervous systems, at least in Hymenoptera. In this study, we evaluated a gynandromorphic individual of bumblebee (Bombus ignitus) with a bilaterally dimorphic head and thorax (left side, male; right side, female) and a uniformly masculine gaster. The gynandromorph exhibited abnormal sexual behavior; it normally approached and touched virgin queens but rarely made subsequent copulation attempt. Dissection of the gaster indicated that it possessed a set of male reproductive organs. We analyzed the encephalic and antennal expression patterns of the fruitless (fru) gene, which shows sex-specific alternative splicing conserved in various insect orders and has been thought to act as the master regulator of sexual behavior in male nervous systems. The gynandromorph showed left-side-biased expression of male-type fru transcripts. We discuss a possible mechanism for the observed unusual interruption of sexual behavior of the gynandromorph by reference to the fru expression pattern and our recent findings on the sexually dimorphic response to female-derived pheromones.

Genetics of biologically based psychological differences.

In recent years, substantial effort has gone into disentangling the genetic contribution to individual differences in behaviour (such as personality and temperament traits). Heritability estimates from twin and family studies, and more recently using whole genome approaches, suggest a substantial genetic component to these traits. However, efforts to identify the genes that influence these traits have had relatively little success. Here, we review current work investigating the heritability of individual differences in behavioural traits and provide an overview of the results from genome-wide association analyses of these traits to date. In addition, we discuss the implications of these findings for the potential applications of Mendelian randomization.This article is part of the theme issue ‘Diverse perspectives on diversity: multi-disciplinary approaches to taxonomies of individual differences'.

Correction: Early postnatal vocalizations predict sociability and spatial memory in C57BL/6J mice: Individual differences in behavioral traits emerge early in development.

[This corrects the article DOI: 10.1371/journal.pone.0186798.].

Early postnatal vocalizations predict sociability and spatial memory in C57BL/6J mice: Individual differences in behavioral traits emerge early in development

The understanding of individual diversity and its link to brain functions is a fundamental issue in neurobiology. Studies in mice have mainly focused on the investigation of behavior traits in adulthood, whereas longitudinal analyses are largely uninvestigated. Here we have conducted systematic behavior tests in individual mice (C57BL6/J, male), comparing phenotypes at early postnatal stages and in adulthood. Each animal showed different scores in individual behavior tests. However, we observed an inverse correlation between repetitive behavior in the Morris water maze test and sociability in the 3-chamber social interaction test; an increase in repetitive behaviors was associated with poor sociability. In longitudinal analyses, the emission of ultrasonic vocalization during maternal separation at postnatal day 6 in pups was correlated positively with sociability and negatively with spatial memory. Our results show a possibility that individual differences in communication between pups and their mother in infancy is a predictive indicator for sociability and cognitive performance as an adult.

Cognitive test batteries in animal cognition research: evaluating the past, present and future of comparative psychometrics.

For the past two decades, behavioural ecologists have documented consistent individual differences in behavioural traits within species and found evidence for animal "personality". It is only relatively recently, however, that increasing numbers of researchers have begun to investigate individual differences in cognitive ability within species. It has been suggested that cognitive test batteries may provide an ideal tool for this growing research endeavour. In fact, cognitive test batteries have now been used to examine the causes, consequences and underlying structure of cognitive performance within and between many species. In this review, we document the existing attempts to develop cognitive test batteries for non-human animals and review the claims that these studies have made in terms of the structure and evolution of cognition. We argue that our current test battery methods could be improved on multiple fronts, from the design of tasks, to the domains targeted and the species tested. Refining and optimising test battery design will provide many benefits. In future, we envisage that well-designed cognitive test batteries may provide answers to a range of exciting questions, including giving us greater insight into the evolution and structure of cognition.

Early social environment influences the behaviour of a family-living lizard.

Early social environment can play a significant role in shaping behavioural development. For instance, in many social mammals and birds, isolation rearing results in individuals that are less exploratory, shyer, less social and more aggressive than individuals raised in groups. Moreover, dynamic aspects of social environments, such as the nature of relationships between individuals, can also impact the trajectory of development. We tested if being raised alone or socially affects behavioural development in the family-living tree skink, Egernia striolata. Juveniles were raised in two treatments: alone or in a pair. We assayed exploration, boldness, sociability and aggression repeatedly throughout each juvenile's first year of life, and also assessed social interactions between pairs to determine if juveniles formed dominant–subordinate relationships. We found that male and/or the larger skinks within social pairs were dominant. Developing within this social environment reduced skink growth, and subordinate skinks were more prone to tail loss. Thus, living with a conspecific was costly for E. striolata. The predicted negative effects of isolation failed to materialize. Nevertheless, there were significant differences in behavioural traits depending on the social environment (isolated, dominant or subordinate member of a pair). Isolated skinks were more social than subordinate skinks. Subordinate skinks also became more aggressive over time, whereas isolated and dominant skinks showed invariable aggression. Dominant skinks became bolder over time, whereas isolated and subordinate skinks were relatively stable in their boldness. In summary, our study is evidence that isolation rearing does not consistently affect behaviour across all social taxa. Our study also demonstrates that the social environment plays an important role in behavioural development of a family-living lizard.

Larval personality does not predict adult personality in a holometabolous insect

Although personality (consistent inter-individual differences in behavioural traits across time and/or contexts) and behavioural syndromes (suites of correlated personality traits) have been widely studied in the last decades, the origin and development of these traits during ontogeny are still underexplored. In this context, species undergoing metamorphosis are of special interest. To date, however, the persistence of personality traits has been only little investigated in organisms undergoing complete metamorphosis such as in holometabolous insects, although this kind of studies may provide important insights from a functional point of view. Here, we tested whether the personality and the behavioural syndrome are maintained through metamorphosis in Tenebrio molitor, a holometabolous insect species. We found that personality and behavioural syndrome were present in both larval and adult stages. However, larval personality and behavioural syndrome did not predict adult behaviour. We suggest that the complete reorganization during metamorphosis may have profound effect on the behaviour of the beetles. These results challenge the established common thought that personality should persist along an individual lifespan.

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.

Drivers of variation in species impacts for a multi-host fungal disease of bats.

Disease can play an important role in structuring species communities because the effects of disease vary among hosts; some species are driven towards extinction, while others suffer relatively little impact. Why disease impacts vary among host species remains poorly understood for most multi-host pathogens, and factors allowing less-susceptible species to persist could be useful in conserving highly affected species. White-nose syndrome (WNS), an emerging fungal disease of bats, has decimated some species while sympatric and closely related species have experienced little effect. We analysed data on infection prevalence, fungal loads and environmental factors to determine how variation in infection among sympatric host species influenced the severity of WNS population impacts. Intense transmission resulted in almost uniformly high prevalence in all species. By contrast, fungal loads varied over 3 orders of magnitude among species, and explained 98% of the variation among species in disease impacts. Fungal loads increased with hibernating roosting temperatures, with bats roosting at warmer temperatures having higher fungal loads and suffering greater WNS impacts. We also found evidence of a threshold fungal load, above which the probability of mortality may increase sharply, and this threshold was similar for multiple species. This study demonstrates how differences in behavioural traits among species-in this case microclimate preferences-that may have been previously adaptive can be deleterious after the introduction of a new pathogen. Management to reduce pathogen loads rather than exposure may be an effective way of reducing disease impact and preventing species extinctions.This article is part of the themed issue 'Tackling emerging fungal threats to animal health, food security and ecosystem resilience'.

Individual variation in an acute stress response reflects divergent coping strategies in a large herbivore

Individuals differ in the manner that they cope with risk. When these behavioral differences are manifested in risky or challenging environments (i.e. stressful situations), they are generally interpreted within the “coping style” framework. As studying inter-individual variability in behavior is particularly challenging in the wild, we used a captive facility to explore consistency in the individual behavioral response to an acute stress in roe deer (Capreolus capreolus). Using behavioral and physiological parameters measured six times across a calendar year, we first quantified individual repeatability and, second, explored the correlations among these parameters that might indicate a coherent stress response. Finally, we analyzed the link between the stress response and individual body mass, a reliable indicator of phenotypic quality in roe deer. We found that the measured parameters were highly repeatable across seasons, indicating that the individual stress response is consistent over time. Furthermore, there was considerable covariation among the stress response parameters, describing a proactivity-reactivity gradient at the individual level. Finally, proactive individuals had higher body mass than reactive individuals. We suggest that consistent individual differences in energy metabolism and physiology may promote consistent individual differences in behavioral traits, providing a mechanistic link between food acquisition tactics and demographic performance.

Perceived relevance of selected behavioural traits in horses – A survey conducted in Sweden

In the present study, a web-based questionnaire was used with the aim to investigate perceived relevance of 14 behavioural traits in horses regarding quality of match between horse and rider. The responses of approximately 2800 participants indicate a high interest in the topic. All traits were considered relevant by at least 50% of the respondents. ‘Easy to bring to new environments’ was the trait indicated as relevant by the highest proportion (85%) of respondents, followed by ‘spirited and forward’ (84%) and ‘tolerant towards humans’ (80%). Respondents’ age as well as preferred equitation discipline was shown to have a profound influence on perception of relevance (P < 0.05). The results suggest a need for methods to objectively evaluate individual differences in behavioural traits to enable selection of horses to optimize horse–rider match.

Behavioural phenotypes over the lifetime of a holometabolous insect.

Introduction: Behavioural traits can differ considerably between individuals, and such differences were found to be consistent over the lifetime of an organism in several species. Whether behavioural traits of holometabolous insects, which undergo a metamorphosis, are consistent across ontogeny is virtually unexplored. We investigated several behavioural parameters at five different time points in the lifetime of the holometabolous mustard leaf beetle Phaedon cochleariae (Coleoptera: Chrysomelidae), two times in the larval (second and third larval stage) and three times in the adult stage. We investigated 1) the stability of the behavioural phenotype (population level), 2) whether individuals rank consistently across behavioural traits and over their lifetime (individual level), and 3) in how far behavioural traits are correlated with the developmental time of the individuals.Results: We identified two behavioural dimensions in every life stage of P. cochleariae, activity and boldness (population level). Larvae and young adults ranked consistently across the investigated behavioural traits, whereas consistency over time was only found in adults but not between larvae and adults (individual level). Compared to adult beetles, larvae were less active. Moreover, younger larvae were bolder than all subsequent life stages. Over the adult lifetime of the beetles, males were less active than females. Furthermore, the activity of second instar larvae was significantly negatively correlated with the development time.Conclusions: Our study highlights that, although there is no individual consistency over the larval and the adult life stage, the behavioural clustering shows similar patterns at all tested life stages of a holometabolous insect. Nevertheless, age- and sex-specific differences in behavioural traits occur which may be explained by different challenges an individual faces at each life stage. These differences are presumably related to the tremendous changes in life-history traits from larvae to adults and/or to a niche shift after metamorphosis as well as to different needs of both sexes, respectively. A faster development of more active compared to less active second instar larvae is in line with the pace-of-life syndrome. Overall, this study demonstrates a pronounced individuality in behavioural phenotypes and presumably adaptive changes related to life stage and sex.

Plasticity in behavioural responses and resistance to temperature stress in Musca domestica

Organisms can respond to and cope with stressful environments in a number of ways including behavioural, morphological and physiological adjustments. To understand the role of behavioural traits in thermal adaptations we compared heat resistance, locomotor (walking and flying) activity, flight performance and morphology of three European populations of Musca domestica (Diptera: Muscidae) originating from different thermal conditions (Spain, Switzerland and Denmark) at benign and stressful high temperatures. Spanish flies showed greater heat resistance than Swiss and Danish flies. Similarly, at the stressful high temperature Spanish flies flew the furthest and Danish flies the shortest distance. Neither body size nor wing loading affected flight performance, although flies with narrower wings tended to fly further (wing shape effect). Swiss flies were most active in terms of locomotor activity at the benign temperature, whereas the Spanish flies were able to stay active for longer at the stressful temperature. Population differences in behavioural traits and heat resistance were obtained using flies held for several generations in a laboratory common garden setting; therefore we suggest that exposure to and avoidance of high temperatures under natural conditions has been an important selective agent causing the suggested adaptive differentiation between the populations.

Differences in behavioural traits between two potentially invasive amphipods, Dikerogammarus villosus and Gammarus pulex

The behavioural trait axes of activity, exploration, boldness and sociability can help to understand the tendency of an invasive species to disperse, as may be expected at the fringe of an invasive population, or to socialise, as may be expected in well-established populations where densities of invaders are typically high. We compared behavioural traits between the gammarids Dikerogammarus villosus and Gammarus pulex from centre and fringe populations at Barton Broad, Norfolk, UK. Dikerogammarus villosus is invasive in Western Europe and has displaced many macroinvertebrate species, including the native G. pulex. Gammarus pulex is itself invasive in Northern Ireland and the Isle of Man, thus its displacement increases interest into what unique characteristics of D. villosus make it a dominantly successful invader. Dikerogammarus villosus was significantly less active, less explorative, and more social than G. pulex. We found no significant differences in the behaviours of D. villosus individuals from the central population and the invasive fringe. These patterns indicate active dispersal is likely important to the invasion success of G. pulex, while D. villosus might depend on passive movement. Our data suggest that behavioural factors determining invasive success within closely related taxa can differ considerably, and may lead to different patterns of invasion.

Subgroup-dependent effects of voluntary alcohol intake on behavioral profiles in outbred Wistar rats

Experimental animal models are critical for understanding the genetic, environmental and neurobiological underpinnings of alcohol use disorders. Limited studies investigate alcohol-induced effects on behavior using free-choice paradigms. The aims of the present experiment were to study voluntary alcohol intake using a modified intermittent access paradigm, investigate the effects of voluntary alcohol intake on behavioral profiles in water- and alcohol-drinking rats, and select extreme low- and high-drinking animals for a more detailed behavioral characterization. Sixty outbred male Wistar rats were randomized into water and alcohol groups. Behavioral profiles in the multivariate concentric square field™ (MCSF) test were assessed prior to and after voluntary alcohol intake. The animals had intermittent access to 20% alcohol and water for three consecutive days per week for seven weeks. The results revealed increased alcohol intake over time. No major alcohol-induced differences on behavior profiles were found when comparing water- and alcohol-drinking animals. The high-drinking animals displayed an alcohol deprivation effect, which was not found in the low-drinking animals. High-drinking rats had lower risk-taking behavior prior to alcohol access and lower anxiety-like behavior after voluntary alcohol intake compared to low-drinking rats. In conclusion, the modified intermittent access paradigm may be useful for pharmacological manipulation of alcohol intake. With regard to behavior, the present findings highlights the importance of studying subgroup-dependent differences and add to the complexity of individual differences in behavioral traits of relevance to the vulnerability for excessive alcohol intake.

Rockiness determines meso-scale conservation of butterflies in Afro-montane grassland

Understanding how and why certain species respond to various habitat resources can optimize conservation strategies. Furthermore, behaviour can contribute significantly to predicting the presence or absence of a species under certain habitat conditions. There is a measurable interaction between higher percentage rock exposure in a landscape and butterfly species richness and composition in montane grasslands. Here, we attempt to explain this interaction by measuring the behavioural responses of montane butterfly species to rock cover. The butterfly assemblage was observed across three increasing levels of rockiness in the landscape. At sites within each of these rockiness categories, we also sampled the different behavioural traits of the different species. We determined whether there were significant differences in behavioural traits among this assemblage in response to rockiness. We also identified the specific species which were responsible for driving differential behavioural responses under varying rock exposure in a landscape. The rockiest areas had significantly more behavioural events, and these behaviours were more often associated with direct utilization of rocks, and related to agonistic interaction. Certain butterfly species therefore use rocks as a utility habitat resource, in different ways, highlighting the importance of the resource-based habitat concept for conservation. As such, for butterfly conservation in these montane grasslands, emphasis is placed on including a rocky gradient in protected areas and conservation landscape designs.

Behavioural type, status and social context affect behaviour and resource allocation in cooperatively breeding cichlids

Individuals often show consistent differences in behavioural traits that may belong to a behavioural syndrome. Aggressive propensity is usually an important component of consistent behavioural types, potentially generating benefits in resource competition with conspecifics that may be traded off against costs in other contexts (e.g. acquisition of mates or coexistence with group members). Such trade-offs have not yet been studied in highly social species. We investigated how aggressive propensity influences competition for dominance, shelters and mates in the cooperatively breeding cichlid Neolamprologus pulcher. Following an established protocol we compared growth trajectories of groups of four fish either matched or unmatched for aggressive type. Furthermore, we analysed social interactions, the acquisition of shelter and possible mating partners (by proximity to shelters and prospective mates) according to aggressive type, showing either high or low aggression levels. Contrary to prediction we found that differences in behavioural idiosyncrasies affected the likelihood of obtaining the dominant position and high-quality territories only marginally. Social interactions, growth rates and body reserve accumulation were affected by behavioural differences. However, the patterns observed in this experiment differed from previous studies and suggest a modulating effect of the social environment on the link between behavioural types and life history decisions. Hence, we suggest that in future studies this relationship should be thoroughly investigated under varying social contexts, especially in highly social species.

Personality traits, reproductive behaviour and alternative mating tactics in male European bitterling, Rhodeus amarus

Individual differences in behavioural traits may play a role in reproductive behaviour and it is likely that different personality types have different reproductive success across specific social environments. This suggests a role for sexual selection for personality types, including a link between behavioural traits and alternative reproductive tactics. While research on morphological differences between guarders (bourgeois males defending resources) and sneakers (males parasitizing the territories of bourgeois males) is well characterized, the role of personality in the adoption of alternative mating tactics has hitherto been largely ignored. We investigated individual behavioural differences in a sneaker‐guarder mating system using size/age-matched males of a small freshwater fish, the European bitterling (Rhodeus amarus). We predicted distinct behavioural responses by guarder and sneaker males that were consistent in different contexts, indicating the existence of behavioural syndromes associated with male mating tactic. No behavioural syndromes were detected in male R. amarus, despite ability of individual male bitterling to establish dominance, boldness and investment in sperm competition being relatively repeatable across three consecutive trials. Male aggression, though not repeatable, was negatively correlated with the number of ejaculations, indicating a trade-off between aggression and sperm loading. No association between the tendency of males to guard a territory and behavioural traits was found, despite a significant association between the tendency to guard and morphological and physiological traits, with higher relative testis size and more breeding tubercles in guarder males. Our data suggest male bitterling mating tactics are largely unconstrained by innate factors and likely to be the product of prevailing environmental and social conditions.

Examination of boldness traits in sexual and asexual mollies (Poecilia latipinna, P. formosa)

Considering the high costs of sexual reproduction (e.g., the production of males), its maintenance and predominance throughout the Animal Kingdom remain elusive. Especially the mechanisms allowing for a stable coexistence of closely related sexual and asexual species are still subject to a lively debate. Asexuals should rapidly outnumber sexuals due to higher population growth rates, unless they face some disadvantages. Here, we investigate potential differences in feeding behavior in a system of sexual (sailfin mollies, Poecilia latipinna) and coexisting gynogenetic fishes (Amazon mollies, Poecilia formosa). In two different experiments, we tested for differences in behavioral traits associated with boldness. Bold individuals take higher risks for gains in resources, so shyer individuals should be less competitive. Our study was motivated by the recent finding that P. formosa are less likely to be preyed upon by piscine predators than P. latipinna. We asked whether this result is indicative of low boldness in P. formosa. However, no differences between the two species were detectible in our behavioral experiments measuring (a) time to emerge from shelter to explore a novel environment, (b) latency time until feeding in a novel environment, and (c) recovery time until feeding restarted after a simulated predator attack. Furthermore, different boldness measures were not correlated with each other within individuals.

The influence of predator regime on the behaviour and mortality of a freshwater amphipod, Gammarus pulex

In species with restricted dispersal, traits may become genetically fixed leading to local adaptations. Therefore, predator avoidance in a prey species may differ between populations experiencing different predator regimes, but also between sexes within a population due to different vulnerability to predators. In this study we used male and female Gammarus pulex from two different predator regimes: fishless ponds, where invertebrates are the dominant predators and ponds with predatory fish. In the laboratory we examined refuge use, mortality, leaf decomposition rate and pair-formation in G. pulex when exposed to predator cues from either invertebrate predators or fish. Individuals from fish ponds spent more time in refuge and had a higher mortality than those from fishless ponds independent of predator cues. There was no effect of pond predator regime or predator cues on leaf decomposition rates. Further, fewer individuals formed pairs in G. pulex from fish ponds than from fishless ponds. Male G. pulex had a higher mortality and a higher decomposition rate than females independent of predator cues. However, there was no difference in refuge use between sexes. Our study shows that there are general differences in behaviour traits, both between predator regimes and sexes in G. pulex.