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

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

Components of variance underlying fitness in a natural population of the great tit Parus major

Traits that are closely associated with fitness tend to have lower heritabilities (h2) than those that are not. This has been interpreted as evidence that natural selection tends to deplete genetic variation more rapidly for traits more closely associated with fitness (a corollary of Fisher's fundamental theorem), but Price and Schluter (1991) suggested the pattern might be due to higher residual variance in traits more closely related to fitness. The relationship between 10 different traits for females, seven traits for males, and overall fitness (lifetime recruitment) was quantified for great tits (Parus major) studied in their natural environment of Wytham Wood, England, using data collected over 39 years. Heritabilities and the coefficients of additive genetic and residual variance (CVA and CVR, respectively) were estimated using an "animal model." For both males and females, a trait's correlation (r) with fitness was negatively related to its h2 but positively related to its CVR. The CVA was not related to the trait's correlation with fitness in either sex. This is the third study using directly measured fitness in a wild population to show the important role of residual variation in determining the pattern of lower heritabilities for traits more closely related to fitness.     

How to become large quickly: quantitative genetics of growth and foraging in a flush feeding lepidopteran larva

Rapid larval growth in insects may be selected for by rapid ephemeral phenological changes in food resources modifying the structure of phenotypic and genetic (co)variation in and among individual traits. We studied the relative effects of three processes which can modify expression of additive genetic and nongenetic variation in traits. First, natural selection tends to erode genetic variation in fitness-related traits. Second, there may be high variance even in traits closely coupled with fitness, if these traits are themselves products of variable lower level traits. Third, traits may be canalized by developmental processes which reduce phenotypic variation. Moreover, we investigated the phenotypic and genetic role played by the underlying traits in attaining simultaneously both large size and short development time. We measured phenotypic and genetic (co)variation in several pre- and post-ingestive foraging traits, growth, development rate, development time and size, together forming a hierarchical network of traits, in the larvae of a flush feeding geometrid, Epirrita autumnata. Rapid larval growth rate and high pupal mass are closely related to fitness in E. autumnata. Traits closely associated with larval growth displayed low levels of additive genetic variation, indicating that genetic variability may have been exhausted by selection for rapid growth. The body size of E. autumnata, in spite of its close correlation with fitness, exhibited a significant additive genetic variation, possiblye because caterpillar size is the outcome of many underlying heritable traits. The low level traits in the hierarchical net, number (indicating larval movements) and size of feeding bouts in leaves, relative consumption rate and efficiency of conversion of ingested food, displayed high levels of residual variation. High residual variation in consumption and physiological ability to handle leaf material resulted from their flexibility which reduced variation in growth rate, i.e. growth rate was canalized. We did not detect a trade-off between development time and final size. On the contrary, large pupal masses were attained by short larval periods, and this relationship was strongly genetically determined, suggesting that both developmental time and final size are expressions of the same developmental process (vigorous growth) and the same genes (or linkage disequilibrium).     

Experimental evidence that adult antipredator behaviour is heritable and not influenced by behavioural copying in a wild bird

Knowledge of the relative importance of genetics and behavioural copying is crucial to appraise the evolvability of behavioural consistencies. Yet, genetic and non-genetic factors are often deeply intertwined, and experiments are required to address this issue. We investigated the sources of variation of adult antipredator behaviour in the Alpine swift (Apus melba) by making use of long-term behavioural observations on parents and cross-fostered offspring. By applying an 'animal model' approach to observational data, we show that antipredator behaviour of adult Alpine swifts was significantly repeatable over lifetime (r = 0.273) and heritable (h(2) = 0.146). Regression models also show that antipredator behaviours differed between colonies and sexes (females were more tame), and varied with the hour and year of capture. By applying a parent-offspring regression approach to 59 offspring that were exchanged as eggs or hatchlings between pairs of nests, we demonstrate that offspring behaved like their biological parents rather than like their foster parents when they were adults themselves. Those findings provide strong evidence that antipredator behaviour of adult Alpine swifts is shaped by genetics and/or pre-hatching maternal effects taking place at conception but not by behavioural copying.     

Do female collared lizards change field use of maximal sprint speed capacity when gravid?

Locomotor ability is well-documented to decrease in gravid female lizards. However, no studies have examined what proportion of maximal sprint speed capacity gravid females use in nature or how a reduction in maximal capacity translates to changes in sprint speeds used in nature. Gravid females may compensate for reduced locomotor ability by increasing the proportion of their maximal capacity used in nature, or by changing their antipredator behaviour. I measured maximal sprint speed in the laboratory for female collared lizards (Crotaphytus collaris) while gravid and nongravid and then compared those to speeds used in the field while foraging and escaping predators, and also while gravid and nongravid. Females had significantly lower maximal sprint speed capacity while gravid, and they ran slower while foraging and escaping predators. However, gravid females did not increase the proportion of maximal capacity used in those contexts compared to when not gravid. Gravid females compensated for reduced locomotor capacity by staying closer to refugia but not by remaining more cryptic. These results suggest that the costs of reduced locomotor capacity may not be associated with direct costs while foraging or escaping predators, but instead with potential indirect effects associated with the change in antipredator behaviour.     

Non‐consumptive effects of predation: does perceived risk strengthen the genetic integration of behaviour and morphology in stickleback?

Predators can shape genetic correlations in prey by altering prey perception of risk. We manipulated perceived risk to test whether such non‐consumptive effects tightened behavioural trait correlations in wild‐caught stickleback from high‐ compared to low‐risk environments due to genetic variation in plasticity. We expected tighter genetic correlations within perceived risk treatments than across them, and tighter genetic correlations in high‐risk than in low‐risk treatments. We identified genetic variation in plasticity, with genetic correlations between boldness, sociality, and antipredator morphology, as expected, being tighter within treatments than across them, for both of two populations. By contrast, genetic correlations did not tighten with exposure to risk. Tighter phenotypic correlations in wild stickleback may thus arise because predators induce correlational selection on environmental components of these traits, or because predators tighten residual correlations by causing environmental heterogeneity that is controlled in the laboratory. Our study places phenotypic integration firmly into an ecological context.     

Sex‐Specific Associations Between Nest Defence,Exploration and Breathing Rate in Breeding Pied Flycatchers

Correlations between behavioural traits constrain animals to a limited range of behavioural choices and set a limit to the available variation in behavioural phenotype of a population. These constraints are especially important during stressful situations, potentially limiting the ability to cope with stress appropriately. As yet, very little consideration has been given to a possible role for sexual selection in maintaining differences in behavioural stability within individuals: sex‐specific differences in behavioural correlations have been seldom studied, especially in the wild. In this field study, we investigated associations between neophobia (latency to enter nest in the presence of a novel object), nest defence (response to a model predator) and breathing rate in response to handling in breeding pied flycatchers (Ficedula hypoleuca). We did not find any significant difference in antipredator responses between males and females, which indicates low sexual conflict over parental care in the pied flycatcher. However, females were more neophobic than males, while males and females did not differ in their breathing rates. Further, our study demonstrated a strong positive correlation between nest defence behaviour and neophobia in male, but not in female pied flycatchers. Males that defended their nest more had lower breathing rate and higher latency to resume nestling feeding after encountering a predator decoy than males that mobbed less intensely. We found only weak evidence that nest partners might affect each other's behaviour in these contexts.     

Selection,structure and the heritability of behaviour

Characters which are closely linked to fitness often have low heritabilities (V_A/V_P). Low heritabilities could be because of low additive genetic variation (V_A), that had been depleted by directional selection. Alternatively, low heritabilities may be caused by large residual variation (V_R=V_P – V_A) compounded at a disproportionately higher rate than V_A across integrated characters. Both hypotheses assume that each component of quantitative variation has an independent effect on heritability. However, V_A and V_R may also covary, in which case differences in heritability cannot be fully explained by the independent effects of elimination‐selection or compounded residual variation. We compared the central tendency of published behavioural heritabilities (mean=0.31, median=0.23) with morphological and life history data collected by 26 ). Average behavioural heritability was not significantly different from average life history heritability, but both were smaller than average morphological heritability. We cross‐classified behavioural traits to test whether variation in heritability was related to selection (dominance, domestic/wild) or variance compounding (integration level). There was a significant three‐way interaction between indices of selection and variance compounding, related to the absence of either effect at the highest integration level. At lower integration levels, high dominance variance indicated effects of selection. It was also indicated by the low CV_A of domestic species. At the same time CV_R increased disproportionately faster than CV_A across integration levels, demonstrating variance compounding. However, neither CV_R nor CV_A had a predominant effect on heritability. The partial regression coefficients of CV_R and CV_A on heritability were similar and a path analysis indicated that their (positive) correlation was also necessary to explain variation in heritability. These results suggest that relationships between additive genetic and residual components of quantitative genetic variation can constrain their independent direct effects on behavioural heritability.     

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.     

Quantitative genetics of oviposition behaviour and interactions among oviposition traits in the sand cricket

We performed a quantitative genetic study of oviposition behaviours and oviposition traits in the sand cricket Gryllus firmus. Egg survival in crickets depends on the depth at which they are inserted into the soil with the ovipositor. We examined whether egg depth depends on ovipositor length alone, or on both morphological and behavioural traits associated with oviposition. Heritability estimates were high (h² >0.5) for ovipositor length and small (h²=0.2) for oviposition behaviours. Negative genetic correlations between ovipositor length and some behavioural traits (digging depth and the behavioural component of egg depth) indicated compensation between oviposition traits on egg depth. Because of behavioural compensation, females with different ovipositor lengths subject to stabilizing selection on egg depth could have equal fitnesses. Females laid their eggs deeper, and their eggs were marginally more evenly distributed in dry than in wet sand. This suggests adaptive phenotypic plasticity in laying behaviour, but may also result from physical constraints of the substrate on the insertion of the ovipositor. The absence of significant between-family variation in oviposition traits in response to sand moisture indicates low evolutionary potential for phenotypic plasticity in oviposition traits according to soil moisture. In highly unpredictable environments, females could spread the risk of desiccation by laying eggs at different depths independently of environmental conditions (bet hedging). Our results show significant additive genetic influences on the ability of a female to spread risks as measured by genetic variation in egg distribution, suggesting that a bet-hedging strategy of egg laying has the potential to evolve in this population. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Female guppies agree to differ: phenotypic and genetic variation in mate-choice behavior and the consequences for sexual selection

Variation among females in mate choice may influence evolution by sexual selection. The genetic basis of this variation is of interest because the elaboration of mating preferences requires additive genetic variation in these traits. Here we measure the repeatability and heritability of two components of female choosiness (responsiveness and discrimination) and of female preference functions for the multiple ornaments borne by male guppies (Poecilia reticulata). We show that there is significant repeatable variation in both components of choosiness and in some preference functions but not in others. There appear to be several male ornaments that females find uniformly attractive and others for which females differ in preference. One consequence is that there is no universally attractive male phenotype. Only responsiveness shows significant additive genetic variation. Variation in responsiveness appears to mask variation in discrimination and some preference functions and may be the most biologically relevant source of phenotypic and genetic variation in mate-choice behavior. To test the potential evolutionary importance of the phenotypic variation in mate choice that we report, we estimated the opportunity for and the intensity of sexual selection under models of mate choice that excluded and that incorporated individual female variation. We then compared these estimates with estimates based on measured mating success. Incorporating individual variation in mate choice generally did not predict the outcome of sexual selection any better than models that ignored such variation.     

Genetic trade-off between abilities to avoid attack and to mate: a cost of tonic immobility

Consistent individual differences in correlated behaviours across contexts or situations, that is, behavioural syndromes, have recently been identified as an important factor shaping the evolution of behavioural traits, because of their potential for explaining trade-offs in behavioural responses. We examined a genetic link between abilities to mate and to avoid predation from the viewpoint of two genetically correlated behavioural traits; tonic immobility (TI), which is considered to be an antipredator behaviour, and activity levels in the red flour beetle, Tribolium castaneum. Males derived from two strains artificially selected for divergent durations of TI were used in the present study: the L strain (with longer duration and higher frequency of TI) and the S strain (shorter duration and lower frequency of TI). We found that males of the L strain had higher survival rates in predatory environments than those of the S strain, and lower mating success even in predator-free environments. To our knowledge, this is the first empirical study showing a genetic trade-off between abilities to mate and to avoid predation in relation to behavioural syndromes, using individuals exhibiting different behavioural strategies.     

Sexual variation in heritability and genetic correlations of morphological traits in house sparrow (Passer domesticus)

Estimates of genetic components are important for our understanding of how individual characteristics are transferred between generations. We show that the level of heritability varies between 0.12 and 0.68 in six morphological traits in house sparrows (Passer domesticus L.) in northern Norway. Positive and negative genetic correlations were present among traits, suggesting evolutionary constraints on the evolution of some of these characters. A sexual difference in the amount of heritable genetic variation was found in tarsus length, wing length, bill depth and body condition index, with generally higher heritability in females. In addition, the structure of the genetic variance-covariance matrix for the traits differed between the sexes. Genetic correlations between males and females for the morphological traits were however large and not significantly different from one, indicating that sex-specific responses to selection will be influenced by intersexual differences in selection differentials. Despite this, some traits had heritability above 0.1 in females, even after conditioning on the additive genetic covariance between sexes and the additive genetic variances in males. Moreover, a meta-analysis indicated that higher heritability in females than in males may be common in birds. Thus, this indicates sexual differences in the genetic architecture of birds. Consequently, as in house sparrows, the evolutionary responses to selection will often be larger in females than males. Hence, our results suggest that sex-specific additive genetic variances and covariances, although ignored in most studies, should be included when making predictions of evolutionary changes from standard quantitative genetic models.     

Correlated geographic variation in predation risk and antipredator behaviour within a wide‐ranging snake species (Notechis scutatus,Elapidae)

Geographic variation in antipredator behaviour within wide‐ranging species may be driven by both genetic and environmental influences. We quantified antipredator responses in neonatal (laboratory born, n = 555) and adult (field caught, n = 346) tiger snakes (Notechis scutatus) from 11 mainland and island sites in southern Australia. We used these data to test predictions from Bonnet et al.'s hypothesis that the vigour of antipredator responses in this species reflects behavioural plasticity (in turn, driven by an individual snake's exposure to predators during its lifetime) rather than by genetic variation in this trait. We used the number of predator taxa in each area as an index of predator risk. As predicted, adult snakes from predator‐rich areas had more vigorous defensive responses when handled, whereas neonatal behaviour (although also variable among populations) was unrelated to predator species richness. Adult males bit more readily than adult females (as expected from the greater predation exposure of males during mate searching) but no such sex difference was evident in neonates. Although alternative models remain possible, our data are most consistent with the hypothesis that geographic divergence in antipredator tactics within this species primarily reflects developmentally plastic responses to local predation risk.     

Ecology shapes the evolutionary trade‐off between predator avoidance and defence in coral reef butterflyfishes

Antipredator defensive traits are thought to trade‐off evolutionarily with traits that facilitate predator avoidance. However, complexity and scale have precluded tests of this prediction in many groups, including fishes. Using a macroevolutionary approach, we test this prediction in butterflyfishes, an iconic group of coral reef inhabitants with diverse social behaviours, foraging strategies and antipredator adaptations. We find that several antipredator traits have evolved adaptively, dependent primarily on foraging strategy. We identify a previously unrecognised axis of diversity in butterflyfishes where species with robust morphological defences have riskier foraging strategies and lack sociality, while species with reduced morphological defences feed in familiar territories, have adaptations for quick escapes and benefit from the vigilance provided by sociality. Furthermore, we find evidence for the constrained evolution of fin spines among species that graze solely on corals, highlighting the importance of corals, as both prey and structural refuge, in shaping fish morphology.     

Phenotypic integration between antipredator behavior and camouflage pattern in juvenile sticklebacks

Predation is a strong selective force that promotes the evolution of antipredator behaviors and camouflage in prey animals. However, the independent evolution of single traits cannot explain how observed phenotypic variations of these traits are maintained within populations. We studied genetic and phenotypic correlations between antipredator behaviors (shoaling and risk‐taking) and morphology traits (pigmentation and size) in juvenile three‐spined sticklebacks by using pedigree‐based quantitative genetic analysis to test phenotypic integration (or complex phenotype) as an evolutionary response to predation risk. Individuals with strongly melanized (i.e., camouflaged) phenotype and genotype were less sociable to conspecifics, but bolder during foraging under predation risk. Individuals with faster growing phenotype and genotype were bolder, and those with lager eyes were more fearful. These phenotypic integrations were not confounded with correlated plastic responses to predation risk because the phenotypes were measured in naïve fish born in the laboratory, but originated from a natural population with predation pressure. Consistent selection for particular combinations of traits under predation pressure or pleiotropic genes might influence the maintenance of the genetic (co)variations and polymorphism in melanin color, growth trajectory, and behavior patterns.     

Variation in the peacock’s train shows a genetic component

Female peafowl (Pavo cristatus) show a strong mating preference for males with elaborate trains. This, however, poses something of a paradox because intense directional selection should erode genetic variation in the males’ trains, so that females will no longer benefit by discriminating among males on the basis of these traits. This situation is known as the ‘lek paradox’, and leads to the theoretical expectation of low heritability in the peacock’s train. We used two independent breeding experiments, involving a total of 42 sires and 86 of their male offspring, to estimate the narrow sense heritabilities of male ornaments and other morphometric traits. Contrary to expectation, we found significant levels of heritability in a trait known to be used by females during mate choice (train length), while no significant heritabilities were evident for other, non-fitness related morphological traits (tarsus length, body weight or spur length). This study adds to the building body of evidence that high levels of additive genetic variance can exist in secondary sexual traits under directional selection, but further emphasizes the main problem of what maintains this variation.     

Courtship signals and mate choice of the flies of inbred Drosophila montana strains

We studied genetic variation in fly mating signals and mate choice in crosses within and between inbred strains of Drosophila montana. Male songs and the cuticular hydrocarbons of both sexes as well as some of the flies’ behavioural traits differed significantly between strains. This did not, however, cause sexual isolation between strains. In fact, courtship was shorter if the female was courted by a male of a foreign strain than when courted by their own male. Heterosis was found for courtship duration and the carrier frequency of male song. Diallel analysis of male song revealed additive genetic variation in four out of the five traits studied. Two traits showed dominance variation and one of these, carrier frequency, expressed unidirectional dominance with alleles for higher carrier frequency being dominant. Direction of dominance in carrier frequency was the same as the direction of sexual selection exercised by D. montana females on this trait, which suggests that sexual selection could be a driving force in the evolution of song towards a higher carrier frequency.     

Coping with predator stress: interclonal differences in induction of heat-shock proteins in the water flea Daphnia magna

Although predation is a strong selection pressure, little is known about the molecular mechanisms to cope with predator stress. This is crucial to understanding of the mechanisms and constraints involved in the evolution of antipredator traits. We quantified the expression of heat-shock protein 60 (Hsp60), a potential marker for predator stress, in four clones of the water flea Daphnia magna, when exposed to fish kairomones. Expression of Hsp60 induction increased after 6 h and returned to base levels after 24 h of predator stress. This suggests that it is a costly transient mechanism to temporarily cope with novel predator stress, before other defences are induced. We found genetic variation in the fixed levels and in the fish-induced levels of Hsp60, which seemed to be linked to each clone's history of fish predation. Our data suggest that Hsp60 can be considered part of a multiple-trait antipredator defence strategy of Daphnia clones to cope with predator stress.     

Species-specific responses of planktivorous fish to the introduction of a new piscivore: implications for prey fitness

1. Antipredator behaviour by the facultative planktivorous fish species roach (Rutilus rutilus), perch (Perca fluviatilis) and rudd (Scardinius erythrophthalmus) was studied in a multi‐year whole‐lake experiment to evaluate species‐specific behavioural and numerical responses to the stocking of pikeperch (Sander lucioperca), a predator with different foraging behaviour than the resident predators large perch (P. fluviatilis) and pike (Esox lucius). 2. Behavioural responses to pikeperch varied greatly during the night, ranging from reduced activity (roach and small perch) and a shift in habitat (roach), to no change in the habitat use and activity of rudd. The differing responses of the different planktivorous prey species highlight the potential variation in behavioural response to predation risk from species of similar vulnerability. 3. These differences had profound effects on fitness; the density of species that exhibited an antipredator response declined only slightly (roach) or even increased (small perch), whereas the density of the species that did not exhibit an antipredator response (rudd) decreased dramatically (by more than 80%). 4. The maladaptive behaviour of rudd can be explained by a ‘behavioural syndrome’, i.e. the interdependence of behaviours expressed in different contexts (feeding activity, antipredator) across different situations (different densities of predators). 5. Our study extends previous studies, that have typically been limited to more controlled situations, by illustrating the variability in intensity of phenotypic responses to predators, and the consequences for population density, in a large whole‐lake setting.