A Behavioral Syndrome in the Adzuki Bean Beetle: Genetic Correlation Among Death Feigning,Activity, and Mating Behavior

When studying animal behavior, it is often necessary to examine traits as a package, rather than as isolated units. Evidence suggests that individuals behave in a consistent manner across different contexts or over time; that is, behavioral syndromes. We compared locomotor activity levels and mating success between beetles derived from two regimes artificially selected for the duration of death‐feigning behavior in the adzuki bean beetle, Callosobruchus chinensis. The two selection regimes comprised strains with higher (L) and lower (S) intensity (frequency and duration) of death‐feigning behavior, respectively. We found that S strains had higher activity levels than L strains for both sexes, i.e., there is a negative genetic correlation between death feigning and activity. In addition, we found that S strains had higher mating success than L strains, presumably due to higher activity, in males but not in females. We thus demonstrate that death feigning is genetically correlated to mating behavior in males but not females in this species, suggesting that behavioral correlations may not always reflect in the same way in both sexes.     

Death feigning as an adaptive anti‐predator behaviour: Further evidence for its evolution from artificial selection and natural populations

Death feigning is considered to be an adaptive antipredator behaviour. Previous studies on Tribolium castaneum have shown that prey which death feign have a fitness advantage over those that do not when using a jumping spider as the predator. Whether these effects are repeatable across species or whether they can be seen in nature is, however, unknown. Therefore, the present study involved two experiments: (a) divergent artificial selection for the duration of death feigning using a related species T. freemani as prey and a predatory bug as predator, demonstrating that previous results are repeatable across both prey and predator species, and (b) comparison of the death‐feigning duration of T. castaneum populations collected from field sites with and without predatory bugs. In the first experiment, T. freemani adults from established selection regimes with longer durations of death feigning had higher survival rates and longer latency to being preyed on when they were placed with predatory bugs than the adults from regimes selected for shorter durations of death feigning. As a result, the adaptive significance of death‐feigning behaviour was demonstrated in another prey–predator system. In the second experiment, wild T. castaneum beetles from populations with predators feigned death longer than wild beetles from predator‐free populations. Combining the results from these two experiments with those from previous studies provided strong evidence that predators drive the evolution of longer death feigning.     

Drop or fly? Negative genetic correlation between death-feigning intensity and flying ability as alternative anti-predator strategies

A prey animal may have the alternative of flying away or feigning death when it encounters predators. These alternatives have a genetic base as anti-predator strategies in the adzuki bean beetle, Callosobruchus chinensis. A negative genetic correlation between death-feigning intensity and flying ability was found in C. chinensis, i.e. lower flying ability is genetically connected to escaping by dropping from a perch and then feigning death, whereas higher flying ability does not correspond to death-feigning behaviour. Two bidirectional artificial selections for death-feigning duration and flying ability were conducted independently in C. chinensis. The strains selected for shorter (longer) duration of death-feigning had higher (lower) flying ability, while the strains selected for lower (higher) flying ability showed longer (shorter) duration of death-feigning. When the two traits were compared in 21 populations of C. chinensis derived from different geographical regions, a significant negative correlation was found between death-feigning intensity and flying ability. Based on these results, the choice between alternative escaping behaviours in animals is discussed from two points of view: phenotypic plasticity, an individual with two tactics; and pleiotropic genetic correlation, different individuals with opposite strategies.     

Genetic correlation between behavioural traits in relation to death-feigning behaviour

Individuals frequently behave in a consistent manner across time or in different situations. We examined the repeatability of duration of death-feigning anti-predator behaviour when attacked, and then carried out artificial selection for duration to calculate its heritability and examine correlated responses to selection in activity levels, in the confused flour beetle, Tribolium confusum. Three replicates of two strains were established by artificial selection for more than 17 generations: S strains exhibited shorter duration and lower frequency of death feigning while L strains exhibited longer duration and higher frequency of death feigning. Duration of death feigning clearly responded to selection, and significant value of realized heritability was detected in all replicates of the two strains. Examination of locomotor activity levels over a constant period showed that S strains had higher locomotor activity levels than L strains. No significant differences between the sexes were observed. Our study thus demonstrates heritability of death feigning and the existence of a negative genetic correlation between intensity of death feigning and activity level.     

The effect of mass‐rearing on death‐feigning behaviour in the sweet potato weevil (Coleoptera: Brentidae)

The aim of our study was to examine the effect of mass‐rearing, in which there is no exposure to predators, on antipredator traits of insects for improving sterile insect technique programs. The duration of death‐feigning (antipredator behaviour) in sweet potato weevil Cylas formicarius (Summers) (Coleoptera: Brentidae) after mass‐rearing for 71 generations were compared with those in wild strain. There was no significant difference in the duration of death‐feigning between wild and mass‐reared strains. This indicated that the death‐feigning behaviour of mass‐reared strain was maintained for 71 generations even in the absence of predators. We discuss the reasons why death‐feigning behaviour is maintained after mass‐rearing.     

Effects of starvation on death‐feigning in adult Eucryptorrhynchus brandti (Coleoptera: Curculionidae)

In insects, death‐feigning is an effective defence strategy. Eucryptorrhynchus brandti, a major borer pest in China, has a weak flight ability and exhibits obvious death‐feigning behaviour when disturbed. Despite a large number of studies of its biological and ecological properties as well as control methods, the death‐feigning behaviour has not been specifically described. In laboratory conditions, we recorded the survival rate under starvation and feeding conditions and evaluated the effect of starvation on the duration and occurrence of death‐feigning. In a continuous experiment, we examined variation in the death‐feigning duration every day over 7 day. Then, we evaluated the effects of starvation for 3, 6 and 9 day in a non‐continuous experiment and further observed variation in the death‐feigning intensity. We found that starvation significantly affected the survival rate. Survival time was significantly longer in the starvation group than in the feeding group, and females had longer survival times than males (female: 14 day, male: 8 day). In the continuous experiment, starved E. brandti had the longest duration of death‐feigning at 2 day, followed by a significant decrease. In the non‐continuous experiment, the duration and proportion of death‐feigning decreased significantly as the duration of starvation increased and were significantly lower than feeding. These observations suggest that starvation is a non‐negligible factor in the death‐feigning behaviour of E. brandti adults, facilitating the interpretation of future ecological and behavioural data of thanatosis.     

EVALUATING A HYPOTHESIS ABOUT HETEROCHRONY: LARVAL LIFE-HISTORY TRAITS AND JUVENILE HIND-LIMB MORPHOLOGY IN HYLA CRUCIFER

This paper reports the results of an investigation into whether selection on genetically based differences in the timing or rate of development (heterochrony) can give rise to nonadaptive morphological differences among individual frogs. We used a quantitative-genetics approach to examine the relationships among the life-history characters time to metamorphosis and larval-growth rate and a functionally significant morphological features, relative hind-limb length, in the spring peeper, Hyla crucifer. Time to metamorphosis and growth rate had low heritabilities in our population. Morphological traits had moderate heritabilities. There were positive genetic correlations between the life-history traits and the components of relative hind-limb length but no significant correlations with the shape variable itself. We used field observations of pond-drying time and experimental results of selection on growth rate to simulate the correlated responses of hind-limb shape to four reasonable selection regimes on the life-history traits. We found little evidence to suggest that relative hind-limb length would display much of a correlated response to such selection. The differences in relative hind-limb length seen among closely related species or among populations of a single species that appear to be unrelated to performance differences are not obviously explicable as neutral correlated responses to selection on larval traits.     

Intrinsic and Extrinsic Factors Influence Expression of Defensive Behavior in Plains Hog‐Nosed Snakes (Heterodon nasicus)

Animals failing to deter predation are eaten. Among the many deterrents to predation, antipredator behaviors are perhaps the most variable, ranging from active (fight or flight) to passive (immobility). We assessed variation in the expression of a passive defensive behavior, death‐feigning, in Plains Hog‐nosed Snakes (Heterodon nasicus) and predicted that intrinsic and extrinsic factors would influence the duration of this behavior and the latency to its onset. We simulated predatory attacks on 27 snakes encountered in the field, and analyzed the behavioral responses of snakes as a function of differences among individuals (sex and size) and environmental factors (temperature and microhabitat). Larger snakes death‐feigned for longer durations than smaller ones; this relationship was stronger for female snakes than for males. Death feints were initiated sooner when snakes were encountered at higher temperatures. Extrinsic factors had a greater influence on latency to death‐feigning behavior, whereas intrinsic factors more strongly influenced its duration. Because our results involved wild snakes, they provide an improved, highly relevant understanding of individual and environmental factors that regulate the expression of immobile defensive behavior. Furthermore, additional hypotheses can now be proposed that address the evolution of defensive behaviors that leave animals prone to attack.     

Predation and life-history variation in Poecilia reliculata (Cyprinodontiformes: Poeciliidae)

Synopsis Reznick and Endler investigated natural variation in life-history traits of populations of Trinidad guppies exposed to one of three intensities of predation: (i) high predation directed primarily at adults, (ii) moderate predation directed primarily at juveniles, and (iii) low predation. They were able to document significant interpopulational differences in life-history traits associated with this differential predation on a trait-by-trait basis. However, the present extended multivariate analysis indicates that (1) life-history traits do not differ significantly between populations exposed to moderate versus low predation, although both differ greatly from high-predation populations; (2) life-history variation is strongly unifactorial; and (3) despite the importance of predation effects, approximately 17% of the variation in life-history variables cannot be accounted for by predation intensity. Residual variation has no obvious geographical patterns, but instead seems to reflect local environmental variability. Life-history differences between predation regimes are consistent with residual patterns of variation within regimes, suggesting that local variation provides the raw material for extrapolation in response to predation, but also that it influences the direction of correlated change in life-history traits.     

Life-History Characteristics and Colonizing Success in Plants

Successful plant colonizers are characterized by the attributesof weediness but exhibit a variety of life-history traits andgenetic systems. Colonizing success would depend on the abilityof exploiting niches in competition with earlier inhabitants.Within-population genetic variation plays a role in adaptationto new habitats. An experiment with hybrid derivatives froma cross between wild and cultivated soybean species proved thatthe ability to establish seedlings in semi-natural conditionswas genetically controlled, and was loosely correlated withvarious traits. A wild rice species, Oryza perennis, shows perennial-annualcontinuum among populations. The populations markedly differedin life-history traits and niche dimension, as conditioned byseasonal water regime and man's disturbance of the habitats.Intra-populational differentiation was also observed. The datasuggested that various life-history traits are selected as aset.     

Correlation between Olfactory Responses, Dispersal Tendencies, and Life-history Traits of the Predatory Mite Neoseiulus Womersleyi (Acari: Phytoseiidae) of Eight Local Populations

To investigate the relationship between foraging behavior and life-history traits of the predatory mite Neoseiulus womersleyi, the olfactory responses, dispersal ratios from a prey patch, predation rates, fecundity, and developmental times in eight local populations of N. womersleyi were investigated. Significant differences among local populations were found in all these traits except fecundity. None of the life-history traits correlated with foraging behavior. A significant positive correlation was found only between the olfactory response and the dispersal ratio. These results suggested that predatory mites with low olfactory responses would stay in a prey patch longer than predatory mites with high olfactory responses.     

A COMPARISON OF INBREEDING DEPRESSION IN LIFE-HISTORY AND MORPHOLOGICAL TRAITS IN ANIMALS

The current study tests the hypothesis that life-history traits (closely related to fitness) show greater inbreeding depression than morphological traits (less closely related to fitness). The mean and median slope of the standardized coefficient of inbreeding depression (the slope of the linear relationship between F and the trait value) for life-history and morphological traits were compared. Slopes for life-history traits were higher than those for morphological traits. At F = 0.25 (full-sibling mating), life-history traits experienced a median reduction of 11.8% in trait value, whereas morphological traits showed a depression in trait value of approximately 2.2%.     

LABORATORY EVOLUTION OF LIFE-HISTORY TRAITS IN THE BEAN WEEVIL (ACANTHOSCELIDES OBTECTUS): THE EFFECTS OF DENSITY-DEPENDENT AND AGE-SPECIFIC SELECTION

Four types of laboratory populations of the bean weevil (Acanthoscelides obtectus) have been developed to study the effects of density-dependent and age-specific selection. These populations have been selected at high (K) and low larval densities (r) as well as for reproduction early (Y) and late (O) in life. The results presented here suggest that the r- and K-populations (density-dependent selection regimes) have differentiated from each other with respect to the following life-history traits: egg-to-adult viability at high larval density (K > r), preadult developmental time (r > K), body weight (r > K), late fecundity (K > r), total realized fecundity (r > K), and longevity of males (r > K). It was also found that the following traits responded in statistically significant manner in populations subjected to different age-specific selection regimes: egg-to-adult viability (O > Y), body weight (O > Y), early fecundity (Y > O), late fecundity (O > Y), and longevity of females and males (O > Y). Although several life-history traits (viability, body weight, late fecundity) responded in similar manner to both density-dependent and age-specific selection regimes, it appears that underlying genetic and physiological mechanisms responsible for differentiation of the r/K and Y/O populations are different. We have also tested quantitative genetic basis of the bean weevil life-history traits in the populations experiencing density-dependent and age-specific selection. Among the traits traded-off within age-specific selection regimes, only early fecundity showed directional dominance, whereas late fecundity and longevity data indicated additive inheritance. In contrast to age-specific selecton regimes, three life-history traits (developmental time, body size, total fecundity) in the density-sependent regimes exhibited significant dominance effects. Lastly, we have tested the congruence between short-term and long-term effects of larval densities. The comparisons of the outcomes of the r/K selection regimes and those obtained from the low- and high-larval densities revealed that there is no congruence between the selection results and phenotypic plasticity for the analyzed life-history traits in the bean weevil.     

Evidence of Phenotypic and Genetic Relationships between Sociality,Emotional Reactivity and Production Traits in Japanese Quail

The social behavior of animals, which is partially controlled by genetics, is one of the factors involved in their adaptation to large breeding groups. To understand better the relationships between different social behaviors, fear behaviors and production traits, we analyzed the phenotypic and genetic correlations of these traits in Japanese quail by a second generation crossing of two lines divergently selected for their social reinstatement behavior. Analyses of results for 900 individuals showed that the phenotypic correlations between behavioral traits were low with the exception of significant correlations between sexual behavior and aggressive pecks both at phenotypic (0.51) and genetic (0.90) levels. Significant positive genetic correlations were observed between emotional reactivity toward a novel object and sexual (0.89) or aggressive (0.63) behaviors. The other genetic correlations were observed mainly between behavioral and production traits. Thus, the level of emotional reactivity, estimated by the duration of tonic immobility, was positively correlated with weight at 17 and 65 days of age (0.76 and 0.79, respectively) and with delayed egg laying onset (0.74). In contrast, a higher level of social reinstatement behavior was associated with an earlier egg laying onset (-0.71). In addition, a strong sexual motivation was correlated with an earlier laying onset (-0.68) and a higher number of eggs laid (0.82). A low level of emotional reactivity toward a novel object and also a higher aggressive behavior were genetically correlated with a higher number of eggs laid (0.61 and 0.58, respectively). These results bring new insights into the complex determinism of social and emotional reactivity behaviors in birds and their relationships with production traits. Furthermore, they highlight the need to combine animal welfare and production traits in selection programs by taking into account traits of sociability and emotional reactivity.     

Causes of covariation of phenotypic traits among populations

Morphological and life-history traits often vary among populations of a species. Traits generally do not vary independently, but show patterns of covariation that can arise from genetic and environmental influences on phenotype. Covariance of traits may arise at an among-population level when genetically influenced traits diverge among populations in a correlated manner. Genetic correlations caused by pleiotropy and/or gene linkage can cause traits to evolve together, but among-population covariance can also arise among traits that are not genetically correlated. For example, “selective covariance” can arise when natural selection directly causes correlated change in a suite of traits. Similarly, mutation, migration, and drift may also sometimes cause correlated genetic changes among populations. Because covariation of traits among populations can arise by several different processes, the evolution of suites of traits must be interpreted with great caution. We discuss the sources of among-population covariance and illustrate one approach to identifying the sources' using data on floral traits of Dalechampia scandens (Euphorbiaceae).     

LONG-TERM LABORATORY EVOLUTION OF A GENETIC LIFE-HISTORY TRADE-OFF IN DROSOPHILA MELANOGASTER. 1. THE ROLE OF GENOTYPE-BY-ENVIRONMENT INTERACTION

Trade-offs among life-history traits are often thought to constrain the evolution of populations. Here we report the disappearance of a trade-off between early fecundity on the one hand, and late-life fecundity, starvation resistance, and longevity on the other, over 10 yr of laboratory selection for late-life reproduction. Whereas the selected populations showed an initial depression in early-life fecundity, they later converged upon the controls and then surpassed them. The evolutionary loss of the trade-off among life-history traits is considered attributable to the following factors: (1) the existence of differences in the culture regimes of the short- and long-generation populations other than the demographic differences deliberately imposed; (2) adaptation of one or both of these sets of populations to the unique aspects of their culture regimes; (3) the existence of an among-environment trade-off in the expression of early fecundity in the two culture regimes, as reflected in assays that mimic those regimes. The trade-off between early and late-life reproductive success, as manifest among divergently selected populations, is apparent or not depending on the assay environment. This demonstration that strong genotype-by-environment interactions can obscure a fundamental trade-off points to the importance of controlling all aspects of the culture regime of experimental populations and the difficulty of doing so even in the laboratory.     

Strategy Space and the Disturbance Spectrum: A Life-History Model for Tree Species Coexistence

The disturbance spectrum consists of disturbance patterns differing in type, size, intensity, and frequency. It is proposed that tree life-history traits are adaptations to particular disturbance regimes. Four independent axes are proposed to define the dominant dimensions of tree strategy space: shade tolerance, tree height, capacity for vegetative reproduction, and seed dispersal distance. A fitness model was developed to elucidate interactions between the proposed life-history traits. The model shows how alternate life-history sets can coexist when disturbance patterns fluctuate in space and time. Variable disturbance regimes were shown, based on data and simulation results, to enhance species coexistence, as predicted. The strategy space model accurately predicts the number of common tree species for the eastern United States, boreal Canada, and southwestern pi?on-juniper woodlands. The model also provides an explanation for latitudinal gradients in tree species richness in North America and Europe. The proposed model predicts a relationship between disturbance characteristics and the species composition of a forest that allows for the coexistence of large numbers of species. The life-history traits of size, growth rate, life span, shade tolerance, age of reproduction, seed dispersal distance, and vegetative reproduction are all incorporated into the model.     

Diurnal Periodicity of Death-Feigning in Cylas formicarius (Coleoptera: Brentidae)

Diurnal periodicity of death-feigning behavior, or thanatosis, was found in adults of the sweet potato weevil, Cylas formicarius (Fabricius) (Coleoptera: Brentidae). The proportion of death-feigned weevils was significantly lower at night than in the daytime only in males. The duration of death-feint was shorter at night than in the daytime in both sexes. The influences of a weevil's behavior prior to being startled (prestimulus behavior) on the proportion of adults feigning death and on the duration of the death-feint were examined. Resting weevils feigned death more frequently and took a longer duration to recover compared to walking ones. The results suggest that, in general, death-feigning is less frequent in active weevils compared to inactive ones. A cost–benefit relationship of death-feigning behavior is discussed in relation to survival and reproduction of C. formicarius.     

Freezing or death feigning? Beetles selected for long death feigning showed different tactics against different predators

Prey evolve antipredator strategies against multiple enemies in nature. We examined how a prey species adopts different predation avoidance tactics against pursuit or sit‐and‐wait predators. As prey, we used three strains of Tribolium beetles artificially selected for short (short strain) or long (long strain) duration of death feigning, and a stock culture (base population). Death feigning is known to be effective for evading a jumping spider in the case of the long strains, while the present study showed that the long‐strain beetles used freezing against a sit‐and‐wait type predator, Amphibolus venator, in this study. The short‐ strain beetles were more easily oriented toward predators. The time to predation was also shorter in the short strains compared to the long strains. The results showed that, as prey, the short strains displayed the same behavior, escaping, against both types of predators. Traditionally, death feigning has been thought to be the last resort in a series of antipredator avoidance behaviors. However, our results showed that freezing and death feigning were not parts of a series of behaviors, but independent strategies against different predators, at least for long‐strain beetles. We also examined the relationship between a predator''s starvation level and its predatory behavior. In addition, the orientation behavior toward and predation rate on the prey were observed to determine how often the predatory insect attacked the beetles.     

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.