Variation In Behavioral Traits Research Articles

Characterizing the (co)variance of personality traits in female Trinidadian guppies (Poecilia reticulata)

A fundamental question in behavioural and evolutionary ecology is to what degree individual phenotypic traits are variable over time and across ecological contexts and whether they are correlated with each other, as (co)variation in traits determines in part their responses to selection and rate of evolution. A first step to addressing this question is to characterize variation in behavioural traits within and among individuals and their covariation in particular ecological contexts. Here, we ascertained whether adult female guppies (Poecilia reticulata), descendants of wild guppies in Trinidad, are consistent or repeatable in their behaviour over time, such that they exhibit individual ‘personalities’ or behavioural types, and whether their personality traits are inter-correlated. Using a repeated-measures design, we twice assayed individual females for each of three ecologically important behavioural traits, Exploration (of a novel environment), Sociability (shoaling with conspecifics) and Boldness (risk taking), under standardized laboratory conditions. We characterized the among-individual (co)variance structure of each behavioural trait measure, and estimated their respective repeatability and the among-individual correlations between these traits using mixed-effects models. All three traits were found to be significantly repeatable and thus can be considered personality traits. None of the estimated correlations between all possible pairings of the three traits were significantly different from zero. Although adult female Trinidadian guppies from our study population exhibited repeatable personality traits, these traits were not inter-correlated (i.e. did not constitute a behavioural syndrome) and were thus independent of each other. Our findings have important implications for the maintenance of behavioural variation within populations and trait evolution.

Developmental and genetic effects on behavioral and life-history traits in a field cricket.

A fundamental goal of evolutionary ecology is to identify the sources underlying trait variation on which selection can act. Phenotypic variation will be determined by both genetic and environmental factors, and adaptive phenotypic plasticity is expected when organisms can adjust their phenotypes to match environmental cues. Much recent research interest has focused on the relative importance of environmental and genetic factors on the expression of behavioral traits, in particular, and how they compare with morphological and life‐history traits. Little research to date examines the effect of development on the expression of heritable variation in behavioral traits, such as boldness and activity. We tested for genotype, environment, and genotype‐by‐environment differences in body mass, development time, boldness, and activity, using developmental density treatments combined with a quantitative genetic design in the sand field cricket (Gryllus firmus). Similar to results from previous work, animals reared at high densities were generally smaller and took longer to mature, and body mass and development time were moderately heritable. In contrast, neither boldness nor activity responded to density treatments, and they were not heritable. The only trait that showed significant genotype‐by‐environment differences was development time. It is possible that adaptive behavioral plasticity is not evident in this species because of the highly variable social environments it naturally experiences. Our results illustrate the importance of validating the assumption that behavioral phenotype reflects genetic patterns and suggest questions about the role of environmental instability in trait variation and heritability.

Social and anxiety-like behaviors contribute to nicotine self-administration in adolescent outbred rats

Both emotional and social traits interact with genetic factors to influence smoking behavior. We previously established a socially acquired nicotine intravenous self-administration model where social learning of a nicotine-associated odor cue reversed conditioned flavor aversion and promoted nicotine intake. In this study, we first phenotyped ~800 adolescent heterogeneous stock rats in open field, novel object interaction, social interaction, elevated plus maze, and marble burying behaviors. These rats were then phenotyped on socially acquired nicotine self-administration. We found 243 significant correlations between different behavioral tests. Principal component regression analysis found that ~10–20% of the variance in nicotine-related measures, such as intake during the first or the last three fixed-ratio sessions, the progressive ratio session, and reinstatement behavior, can be explained by variations in behavioral traits. Factors corresponding to social behavior and anxiety were among the strongest predictors of nicotine intake and reinstatement of nicotine-seeking behavior. We also found many sex differences in behavioral measures. These data indicated that the genetic diversity of this population, in combination with social behaviour and anxiety, are significant contributors to the divergent nicotine self-administration behavior and indicated a high probability of discovering sex-specific genetic mechanisms for nicotine intake in future genome-wide association studies.

Top-down control by an aquatic invertebrate predator increases with temperature but does not depend on individual behavioral type.

Variation in behavioral traits among individuals within a population can have implications for food webs and ecosystems. Temperature change also alters food web structure and function, but potential interactions between warming and intraspecific behavioral variation are largely unexplored. We aimed to test how increased temperature, individual activity level of a predatory backswimmer (Anisops assimilis), and their interaction influenced the strength of top‐down control of zooplankton and phytoplankton. We used stable isotopes to support our assumption that the study population of A. assimilis is zooplanktivorous, and behavioral trials to confirm that activity level is a repeatable trait. We established freshwater microcosms to test for effects of warming, backswimmer presence, and backswimmer behavioral type on zooplankton density, zooplankton composition, and phytoplankton chlorophyll a. Top‐down control was present and was generally stronger at increased temperature. There was no indication that predator behavioral type influenced the strength of top‐down control either on its own or interactively with temperature. Predator behavioral type may not be associated with ecologically important function in this species at the temporal and spatial scales addressed in this study, but the links between behavior, temperature, and food web processes are worthy of broader exploration.

RETRACTED: Physiology underlies the assembly of ecological communities

Trait-based community ecology promises an understanding of the factors that determine species abundances and distributions across habitats. However, ecologists are often faced with large suites of potentially important traits, making generalizations across ecosystems and species difficult or even impossible. Here, we hypothesize that key traits structuring ecological communities may be causally dependent on common physiological mechanisms and that elucidating these mechanisms can help us understand the distributions of traits and species across habitats. We test this hypothesis by investigating putatively causal relationships between physiological and behavioral traits at the species and community levels in larvae of 17 species of dragonfly that co-occur at the landscape scale but segregate among lakes. We use tools borrowed from phenotypic selection analyses to show that physiological traits underlie activity rate, which has opposing effects on foraging and predator avoidance behaviors. The effect of activity on these behaviors ultimately shapes species distributions and community composition in habitats with either large-bodied fish or invertebrates as top predators. Remarkably, despite the inherent complexity of ecological communities, the expression of just two biomolecules accounts for a high proportion of the variation in behavioral traits and hence, dragonfly community composition between habitats. We suggest that causal relationships among traits can drive species distributions and community assembly.

Behavioral differences within and among populations of an African cichlid found in divergent and extreme environments.

Animals are increasingly faced with human-induced stressors that vary in space and time, thus we can expect population-level divergence in behaviors that help animals to cope with environmental change. However, empirical evidence of behavioral trait divergence across environmental extremes is lacking. We tested for variation in behavioral traits among 2 populations of an African cichlid fish (Pseudocrenilabrus multicolor victoriae Seegers, 1990) that experience extremes of dissolved oxygen (DO) and turbidity and are known to vary in a number of physiological and life history traits associated with these stressors. Using a common garden rearing experiment, F1 progeny from wild-caught parents originating from a swamp (low DO, clear) and a river (high DO, turbid) were reared in high DO, clear water. Predator simulation assays were conducted to test for (1) variation in boldness, general activity, and foraging activity between populations, (2) differences in correlations between behaviors within and across populations, and (3) repeatability of behaviors. There was strong evidence for divergence between populations, with swamp fish being more bold (i.e., leaving refuge sooner after a simulated predator attack) and active (i.e., spent more time out of refuge) than river fish. Across populations there were positive correlations between foraging activity and both boldness and general activity; however, within populations, there was only a strong positive relationship between foraging activity and boldness in the river population. Here, we have demonstrated that populations that originate from drastically different environments can produce progeny that exhibit measurable differences in behaviors and their correlated relationships even when reared under common conditions.

Metabolic Costs of Feeding Predictively Alter the Spatial Distribution of Individuals in Fish Schools

Group living is ubiquitous among animals [1, 2], but the exact benefits of group living experienced by individual groupmates is related to their spatial location within the overall group [3-5]. Individual variation in behavioral traits and nutritional state is known to affect interactions between individuals and their social group [6, 7], but physiological mechanisms underpinning collective animal behavior remain largely unexplored [8]. Here, we show that while fish at the front of moving groups are most successful at capturing food items, these individuals then show a systematic, post-feeding movement toward the rear of groups. Using observations of fish feeding in groups coupled with estimates of metabolic rate in fish consuming different meal sizes, we demonstrate that the magnitude of this shift in spatial position is directly related to the aerobic metabolic scope remaining after accounting for energetic costs of digestion. While previous work has shown that hungry individuals occupy anterior positions in moving groups [9, 10], our results show that the metabolic demand of food processing reduces the aerobic capacity available for locomotion in individuals that eat most, thus preventing them from maintaining leading positions. This basic trade-off between feeding and locomotor capacity could fundamentally dictate the spatial position of individuals within groups, perhaps obviating the role of individual traits in determining spatial preferences over shorter timescales (e.g., hours to days). This may be a general constraint for individuals within animal collectives, representing a key, yet overlooked, mediator of group functioning that could affect leadership, social information transfer, and group decision making.

Proactive behavior, but not inhibitory control, predicts repeated innovation by spotted hyenas tested with a multi-access box.

Innovation is widely linked to cognitive ability, brain size, and adaptation to novel conditions. However, successful innovation appears to be influenced by both cognitive factors, such as inhibitory control, and non-cognitive behavioral traits. We used a multi-access box (MAB) paradigm to measure repeated innovation, the number of unique innovations learned across trials, by 10 captive spotted hyenas (Crocuta crocuta). Spotted hyenas are highly innovative in captivity and also display striking variation in behavioral traits, making them good model organisms for examining the relationship between innovation and other behavioral traits. We measured persistence, motor diversity, motivation, activity, efficiency, inhibitory control, and neophobia demonstrated by hyenas while interacting with the MAB. We also independently assessed inhibitory control with a detour cylinder task. Most hyenas were able to solve the MAB at least once, but only four hyenas satisfied learning criteria for all four possible solutions. Interestingly, neither measure of inhibitory control predicted repeated innovation. Instead, repeated innovation was predicted by a proactive syndrome of behavioral traits that included high persistence, high motor diversity, high activity and low neophobia. Our results suggest that this proactive behavioral syndrome may be more important than inhibitory control for successful innovation with the MAB by members of this species.

Selection as a domain-general evolutionary process

The behavioral phenotype of an organism results from selective processes acting on variation in behavioral traits during ontogeny (during life span) and phylogeny (across generations). Different adaptive processes can be categorized as environment-phenotype feedback loops. In this cross-disciplinary approach, we discuss the interaction of ontogenetic selective processes, traditionally studied by behavior analysts, and phylogenetic selection processes, traditionally studied by biologists. We elaborate upon the Extended Evolutionary Synthesis by addressing the connection between selection as a domain-general process and phenomena such as classical and operant conditioning, imprinting, adjunctive behavior, and gene-culture coevolution. Selection is in this context understood as a dynamic iterative feedback loop producing a phenotype beyond the strict morphotype. The extended phenotype is related to the concept of niche construction in which the behavior of organisms shapes their environment, which again selects the behavior of the organisms in an iterative process. A discussion of interacting environmental factors selecting human food choice both during phylogeny and ontogeny exemplifies the generality of selection processes acting on behavior.

Investigating large‐scale invasion patterns using‐small scale invasion successions—phenotypic differentiation of the invasive round goby (Neogobius melanostomus) at invasion fronts

AbstractSpecies invasions are an ever‐growing problem that increases with globalization through increased frequency of unintentional introductions. Between establishment and spread, a lag phase often occurs in which population growth is exponential and dispersal frequency low. Individual variation in behavioral traits, consistent through time and context, have been found crucial for understanding ecological processes such as density dependent dispersal during species invasions. In a previous study of the invasive round goby (Neogobius melanostomus), we found population differentiation between old and new populations in the Baltic Sea with individuals in new populations being more asocial, bold, and active. Here, we investigate if behavioral differentiations are created already during the initial spread from newly established populations. Hence, we monitored population growth and subsequent small‐scale spread (< 800 m) in two newly invaded areas, as well as the behavioral traits previously connected to dispersal, over two successional seasons. We found phenotypic differentiation between dispersing and resident individuals with small‐scale dispersers being smaller and more asocial. In addition, our catch‐per‐unit‐effort data suggest a lag‐phase of 3–5 yr, following initial colonization, before the round goby start spreading into the surrounding environment. This suggests that, at least in species that grow to high densities fast, sociability is more important than boldness and activity for triggering density‐dependent dispersal.

High levels of gene flow among song dialect populations of the Puget Sound white‐crowned sparrow

AbstractPopulations within a species can show geographic variation in behavioral traits that affect mating decisions or limit dispersal. This may lead to restricted gene flow, resulting in a correlation between behavioral variation and genetic differentiation. Populations of a songbird that differ in a learned behavioral trait, their song dialects, may also differ genetically. If song dialects function as mating barriers, evolutionary processes such as genetic drift should lead to divergence in allele frequencies among dialect populations. The Puget Sound white‐crowned sparrow (Zonotrichia leucophrys pugetensis) is an excellent study system with a well‐defined series of song dialects along the Pacific Northwest coast. A previous study found low genetic differentiation based on four microsatellite loci; however, available loci and analyses techniques have since dramatically improved and allow us to reassess gene flow in this species. We also add extra samples to fill in gaps and add a new level of analysis of geographic variation. Based on acoustic similarities, we group six song dialects into two geographically larger “northern” and “southern” song themes. One southern dialect is acoustically more similar to dialects in the north, which makes the genetic profile of birds singing this dialect particularly interesting. Traditional F‐statistics, analysis of molecular variance as well as Bayesian techniques confirmed the earlier result that geographic variation in song does not correlate with the neutral genetic structure of the sampled dialect populations. The song themes also did not differ genetically, and the origin of the extralimital northern‐theme dialect cannot be determined. We compare this result to findings in several other species and discuss how the timing of learning and dispersal allow vocalizations to vary independently of patterns of genetic divergence.

Determinants, selection and heritability of docility in wild eastern chipmunks (Tamias striatus)

Many behavioural traits show important inter-individual phenotypic and genetic variation despite strong potential selection that should reduce this variability. Spatial and temporal heterogeneity in environmental conditions has been proposed to maintain such variation but empirical evidences supporting this hypothesis are still scarce for behavioural traits. Here, we analysed the repeatability and the ecological and individual factors that influence the expression of docility across different environmental contexts in wild eastern chipmunks (Tamias striatus) studied over a period of 10 years. We also estimated the heritability of docility and the patterns of viability selection acting on this trait for adults and juveniles. Docility was moderately repeatable among various contexts and was positively affected by age, was higher in males than that in females, was higher during the fall and decreased with population density. Heritability of docility was low at 0.17. We found disruptive selection for the survival of adults only, individuals more or less docile than average having a higher survival. Our study confirms that docility is both phenotypically and genetically variables and that disruptive selection might maintain the variability in this trait. Documenting the factors allowing the maintenance of phenotypic and genetic variation of behavioural traits within natural populations is a central objective in ecology and evolution. Here, we studied a wild eastern chipmunk population over 10 years and recorded docility, a personality trait, on both juveniles and adults. We showed that docility was repeatable and that it was also heritable and influenced by different individual and environmental factors. Importantly, we also found that disruptive viability selection was acting on adult docility independently of environmental variations. Our results show that docility is both phenotypically and genetically variable and that patterns of selection acting on this trait can maintain personality heterogeneity across temporally varying environmental conditions in the wild.

Modelling Autistic Features in Mice Using Quantitative Genetic Approaches.

Animal studies provide a unique opportunity to study the consequences of genetic variants at the behavioural level. Human studies have identified hundreds of risk genes for autism spectrum disorder (ASD) that can lead to understanding on how genetic variation contributes to individual differences in social interaction and stereotyped behaviour in people with ASD. To develop rational therapeutic interventions, systematic animal model studies are needed to understand the relationships between genetic variation, pathogenic processes and the expression of autistic behaviours. Genetic and non-genetic animal model strategies are here reviewed in their propensity to study the underpinnings of behavioural trait variation. We conclude that an integration of reverse and forward genetic approaches may be essential to unravel the neurobiological mechanisms underlying ASD.

Short communication: Genetic variation in choice consistency for cows accessing automatic milking units.

Dairy cows milked in automatic milking systems (AMS) with more than 1 milking box may, as individuals, have a preference for specific milking boxes if allowed free choice. Estimates of quantitative genetic variation in behavioral traits of farmed animals have previously been reported, with estimates of heritability ranging widely. However, for the consistency of choice in dairy cows, almost no published estimates of heritability exist. The hypothesis for this study was that choice consistency is partly under additive genetic control and partly controlled by permanent environmental (animal) effects. The aims of this study were to obtain estimates of genetic and phenotypic parameters for choice consistency in dairy cows milked in AMS herds. Data were obtained from 5 commercial Danish herds (I-V) with 2 AMS milking boxes (A, B). Milking data were only from milkings where both the present and the previous milkings were coded as completed. This filter was used to fulfill a criterion of free-choice situation (713,772 milkings, 1,231 cows). The lactation was divided into 20 segments covering 15d each, from 5 to 305d in milk. Choice consistency scores were obtained as the fraction of milkings without change of box [i.e., 1.0 - µ(box change)] for each segment. Data were analyzed for one part of lactation at a time using a linear mixed model for first-parity cows alone and for all parities jointly. Choice consistency was found to be only weakly heritable (heritability=0.02 to 0.14) in first as well as in later parities, and having intermediate repeatability (repeatability coefficients=0.27 to 0.56). Heritability was especially low at early and late lactation states. These results indicate that consistency, which is itself an indication of repeated similar choices, is also repeatable as a trait observed over longer time periods. However, the genetic background seems to play a smaller role compared with that of the permanent animal effects, indicating that consistency could also be a learned behavior. We concluded that consistency in choices are quantifiable, but only under weak genetic control.

Evolution of bower building in Lake Malawi cichlid fish: phylogeny, morphology, and behavior

Despite considerable research, we still know little about the proximate and ultimate causes behind behavioral evolution. This is partly because understanding the forces acting on behavioral phenotypes requires the study of species-rich clades with extensive variation in behavioral traits, of which we have few current examples. In this paper, we introduce the bower-building cichlids of the Lake Malawi adaptive radiation, a lineage with over 100 species, each possessing a distinct male extended phenotype used to signal reproductive fitness. Extended phenotypes are useful units of analysis for the study of behavior since they are static structures that can be precisely measured within populations. To this end we recognize two core types of bowers - mounds (“castles”) and depressions (“pits”). We employ an established framework for the study of adaptive radiations to ask how traits related to other stages of radiations, macrohabitat and feeding morphology, are associated with the evolution of pit and castle phenotypes. We demonstrate that pits and castles are evolutionarily labile traits and have been derived numerous times in multiple Malawi genera. Using public ecological and phenotypic data sets we find significant and correlated differences in macrohabitat (depth), sensory ability (opsin expression), and feeding style (jaw morphology and biomechanics) between pit-digging and castle-building species. Phylogeny-corrected comparisons also show significant differences in several measures of jaw morphology while indicating non-significant differences in depth. Finally, using laboratory observations we assay courtship behaviors in a pit-digging (Copadichromis virginalis) and a castle-building species (Mchenga conophoros). Together, these results show that traits at multiple biological levels act to regulate the evolution of a courtship behavior within natural populations.

Exploratory and defensive behaviours change with sex and body size in eastern garter snakes (Thamnophis sirtalis)

Phenotypic traits are important to consider when examining behaviour because they can help explain behavioural trait variation. Behaviours such as exploration, boldness, and defense may vary between individuals because different intensities of a behaviour may be advantageous for males versus females, or at different body sizes. We tested the hypothesis that exploration, boldness, and defensive behaviours are related to body size, sex, and reproductive status in eastern garter snakes, Thamnophis sirtalis. We also tested whether the measured behavioural traits were consistent through time (i.e., whether eastern garter snakes could have personalities) and whether the measured behavioural traits were related to one another (i.e., whether behavioural syndromes could be present in eastern garter snakes). Males and non-gravid females were more likely to flee than gravid females when faced with an attack. Males and non-gravid females were also more active after the attack than before the attack, whereas gravid females were more active before the attack. Furthermore, longer females explored less than smaller females, with a more precipitous decline of exploration as a function of size in gravid females than in non-gravid females. In contrast, longer males explored more than smaller males. Although we did not detect behavioural syndromes, within individuals the measured behavioural traits were repeatable through time, suggesting that eastern garter snakes could have personalities.

Nest building and description of parental care behavior in a temperate reef fish, Chromis crusma (Pisces: Pomacentridae)

Subtle ecological and behavioral mechanisms that enhance reproduction such as nest building by animals may provide useful information of population level processes. Variation in behavioral traits may be observed as phenotypic traits that are shaped by sexual and natural selection. Using ecological sampling of benthic substrata and underwater video recordings, we assessed nest-building behavior through habitat modifications, and size of individuals performing parental care behavior and egg/hatching traits of an abundant temperate reef fish, Chromis crusma. We identified that only male individuals performed nest building and uniparental care. We noted that nests containing filamentous green or red algae had the highest percent cover of eggs. Using video recordings, we provided evidence of parental care. Male individuals spent nearly 80% of their time inside the nest, aerating the eggs with their fins and mouth, removing unwanted materials, and defending the nest against conspecific, heterospecific, and other predators. The field-collected eggs, characterized by an oil globule and adhesive filaments, hatched after 7 days in the laboratory. The nest-building and parental care behavior of C. crusma lasted for 3 months, and several nests can be constructed throughout the season. The behavior of building and defending the nests, which is a characteristic of the family members, is a key aspect for the success of the C. crusma; this fish is abundant in kelp ecosystems of the southeastern Pacific.

Invasive cane toads: social facilitation depends upon an individual's personality.

Individual variation in behavioural traits (including responses to social cues) may influence the success of invasive populations. We studied the relationship between sociality and personality in invasive cane toads (Rhinella marina) from a recently established population in tropical Australia. In our field experiments, we manipulated social cues (the presence of a feeding conspecific) near a food source. We captured and compared toads that only approached feeding sites where another toad was already present, with conspecifics that approached unoccupied feeding sites. Subsequent laboratory trials showed correlated personality differences (behavioural syndromes) between these two groups of toads. For example, toads that approached already-occupied rather than unoccupied feeding sites in the field, took longer to emerge from a shelter-site in standardized trials, suggesting these individuals are ‘shy’ (whereas toads that approached unoccupied feeding stations tended to be ‘bold’). Manipulating hunger levels did not abolish this difference. In feeding trials, a bold toad typically outcompeted a shy toad under conditions of low prey availability, but the outcome was reversed when multiple prey items were present. Thus, both personality types may be favored under different circumstances. This invasive population of toads contains individuals that exhibit a range of personalities, hinting at the existence of a wide range of social dynamics in taxa traditionally considered to be asocial.

Individual (co)variation in standard metabolic rate, feeding rate, and exploratory behavior in wild-caught semiaquatic salamanders.

Repeatability is an important concept in evolutionary analyses because it provides information regarding the benefit of repeated measurements and, in most cases, a putative upper limit to heritability estimates. Repeatability (R) of different aspects of energy metabolism and behavior has been demonstrated in a variety of organisms over short and long time intervals. Recent research suggests that consistent individual differences in behavior and energy metabolism might covary. Here we present new data on the repeatability of body mass, standard metabolic rate (SMR), voluntary exploratory behavior, and feeding rate in a semiaquatic salamander and ask whether individual variation in behavioral traits is correlated with individual variation in metabolism on a whole-animal basis and after conditioning on body mass. All measured traits were repeatable, but the repeatability estimates ranged from very high for body mass (R = 0.98), to intermediate for SMR (R = 0.39) and food intake (R = 0.58), to low for exploratory behavior (R = 0.25). Moreover, repeatability estimates for all traits except body mass declined over time (i.e., from 3 to 9 wk), although this pattern could be a consequence of the relatively low sample size used in this study. Despite significant repeatability in all traits, we find little evidence that behaviors are correlated with SMR at the phenotypic and among-individual levels when conditioned on body mass. Specifically, the phenotypic correlations between SMR and exploratory behavior were negative in all trials but significantly so in one trial only. Salamanders in this study showed individual variation in how their exploratory behavior changed across trials (but not body mass, SMR, and feed intake), which might have contributed to observed changing correlations across trials.

Complete mitochondrial genome of the kissing gourami, Helostoma temminkii

The kissing gourami (Helostoma temminkii) belongs to the Labyrinth fishes (Perciformes: Anabantoidei), which exhibits a wide variety of behavioral traits. In this study the complete mitogenome of H. temminkii was determined to be 16,740 bp in length. It contains 13 protein-coding genes, 22 transfer RNA genes and 2 ribosomal RNA genes. The sequence structure of non-coding control region was also analyzed. Comparing the mitochondrial genome of H. temminkii with its closely related species Colisa lalia showed the similarity of 78%. The complete mitochondrial genome of H. temminkii provides resource for phylogenetic analysis on Anabantoidei.