Behavioural phenotypes over the lifetime of a holometabolous insect

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

Match–Mismatch Experiments Using Photoperiod Expose Developmental Plasticity of Personality Traits

Behavioural differences between individuals are often found to be consistent across contexts and/or over time, although recent studies suggest that ontogenetic processes and learning might influence personality. During ontogeny, environmental influences may play an important role in shaping an individual's personality as well as its physiology. Seasonal changes are ubiquitous and known to influence development. To study developmental plasticity, of behaviour and physiology in the wild cavy (Cavia aperea), we manipulated the photoperiod in a fully crossed match–mismatch design by simulating spring and autumn photoperiod until weaning and subsequently moving half of the animals into the mismatching photoperiod. We found developmental plasticity in behavioural and physiological traits before and after sexual maturation for growth, resting metabolic rate and fearlessness. For fearlessness, changes in response to the opposite photoperiod were more pronounced in males than in females. Exploration and boldness were only influenced by early, but not by late photoperiod. No sex differences were found for these two traits. Even though our treatment changed average trait expression, some behavioural traits proved consistent over time, but physiological traits were not. Fearlessness was consistent only in animals that did not change photoperiod during development, whereas exploration and boldness were consistent over time regardless of photoperiodic treatment. Our study shows that in response to a change in photoperiod personality traits differ substantially in developmental plasticity.     

Life-history variation in relation to time constraints in a damselfly

Although variation within populations in plasticity to time constraints is expected with regard to hatching date, empirical studies are largely lacking. We studied life-history responses to time constraints manipulated by photoperiod and associated with hatching date in larvae of the damselfly Lestes viridis for two populations with a different hydroperiod. In a common garden experiment, early- and late-hatched larvae from both populations were reared at two photoperiods mimicking the start and the end of the egg-hatching season. In a reciprocal transplant experiment, early- and late-hatched larvae from both populations were reared in both ponds. In all these experiments, larvae were reared from egg hatching until adult emergence. Within both populations, larvae reared at the photoperiod indicating a late time point in the growing season, reduced development time to compensate for their perceived shorter development period. Growth rate, however, did not respond to photoperiod, resulting in a lower mass at emergence. As expected, both in the laboratory and in the field, larvae from eggs that hatched later in the season generally had a shorter development time and a faster growth rate, resulting in a higher mass at emergence compared to early-hatched larvae. This may explain the intriguing seasonal increase in mass at emergence in this species, and affect the predictions of optimality models. None of these life-history responses differed between the two populations, despite clear differences in time constraints linked to hydroperiod, suggesting the robustness of the observed patterns. Given the ubiquity of asynchronous hatching in nature, and the adaptive value of the observed differences between early- and late-hatched larvae, we expect the effects of hatching date on life-history plasticity to be widespread.     

The Association Between Personality Traits,Morphological Traits and Alternative Mating Behaviour in Male Endler's Guppies,Poecilia wingei

Alternative mating behaviour, personality traits and morphological characters are predicted to be correlated. Bolder, larger and more colourful males are expected to preferentially court females, while shy, small and drab‐coloured individuals are predicted to sneak copulations. We used males of Endler's guppy, Poecilia wingei, to test this association over a long temporal period (hence including ontogenetic changes) and under two social environments (male‐biased and female‐biased). We found that personality traits (exploration, boldness, activity) of P. wingei males were highly repeatable across long time spans, but they were not correlated (formed no behavioural syndrome). Male age and social environment had no effect on any personality trait, despite their effects on alternative mating behaviour. Young males with higher activity levels were more likely to attempt sneaking. In older fish, there was an association between orange coloration, courtship and boldness, but this was not observed in young males. Our results suggest that alternative mating behaviour is more flexible than personality traits and is independent of them. Non‐colour‐based morphological traits (gonopodium length, body length, caudal straps length, dorsal fin length) were not correlated with any particular mating behaviour.     

Personality and the emergence of the pace-of-life syndrome concept at the population level

The pace-of-life syndrome (POLS) hypothesis specifies that closely related species or populations experiencing different ecological conditions should differ in a suite of metabolic, hormonal and immunity traits that have coevolved with the life-history particularities related to these conditions. Surprisingly, two important dimensions of the POLS concept have been neglected: (i) despite increasing evidence for numerous connections between behavioural, physiological and life-history traits, behaviours have rarely been considered in the POLS yet; (ii) the POLS could easily be applied to the study of covariation among traits between individuals within a population. In this paper, we propose that consistent behavioural differences among individuals, or personality, covary with life history and physiological differences at the within-population, interpopulation and interspecific levels. We discuss how the POLS provides a heuristic framework in which personality studies can be integrated to address how variation in personality traits is maintained within populations.     

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

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

Developmental response to a seasonal time constraint: the effects of photoperiod on reproduction in the grasshopper Romalea microptera

Abstract.  1. Some organisms respond adaptively to seasonal time constraints by altering development time to life-history transitions (e.g. metamorphosis, oviposition). Such life-history changes may have costs (e.g. reduced fecundity, mass, offspring quality).
2. The hypothesis that a northern population of the grasshopper Romalea microptera (Beauvois) would show adaptive plasticity in oviposition timing in response to seasonal time constraints was tested by manipulating photoperiod to simulate the middle of the active season (Long photoperiod), the end of the active season (Short photoperiod), and seasonal change (photoperiod Declining from long to short). Females received either high or low food rations. Short or Declining photoperiod were predicted to induce early oviposition with costs of reduced egg number, post-oviposition mass, or egg size, particularly in low-food females.
3. Effects of food ration and photoperiod, but not interaction, were significant in failure time analysis of age at oviposition. mancova on age at oviposition, egg number, and post-oviposition mass yielded similar effects. The multivariate effect of photoperiod resulted primarily from reduced time to oviposition in Short or Declining photoperiod. No costs in egg number or post-oviposition mass were associated with this photoperiod-induced reduction in time to oviposition. The multivariate effect of food ration resulted mainly from lower egg number with low food. Food ration affected egg size, but photoperiod and interaction did not. In all cases, Short and Declining photoperiod produced similar effects.
4. In its northern range, R. microptera accelerates reproduction in response to seasonal constraints, a response that may be adaptive. How R. microptera avoids costs associated with this reduced pre-oviposition period remains unknown.     

Northward range expansion requires synchronization of both overwintering behaviour and physiology with photoperiod in the invasive Colorado potato beetle (Leptinotarsa decemlineata)

Photoperiodic phenological adaptations are prevalent in many organisms living in seasonal environments. As both photoperiod and growth season length change with latitude, species undergoing latitudinal range expansion often need to synchronize their life cycle with a changing photoperiod and growth season length. Since adaptive synchronization often involves a large number of time-consuming genetic changes, behavioural plasticity might be a faster way to adjust to novel conditions. We compared behavioural and physiological traits in overwintering (diapause) preparation in three latitudinally different European Colorado potato beetle (Leptinotarsa decemlineata) populations reared under two photoperiods. Our aim was to study whether behavioural plasticity could play a role in rapid range expansion into seasonal environments. Our results show that while burrowing into the soil occurred in the southernmost studied population also under a non-diapause-inducing long photoperiod, the storage lipid content of these beetles was very low compared to the northern populations. However, similar behavioural plasticity was not found in the northern populations. Furthermore, the strongest suppression of energy metabolism was seen in pre-diapause beetles from the northernmost population. These results could indicate accelerated diapause preparation and possibly energetic adjustments due to temporal constraints imposed by a shorter, northern, growth season. Our results indicate that behavioural plasticity in burrowing may have facilitated initial range expansion of L. decemlineata in Europe. However, long-term persistence at high latitudes has required synchronization of burrowing behaviour with physiological traits. The results underline that eco-physiological life-history traits of insects, such as diapause, should be included in studies on range expansion.     

Life-history evolution when Lestes damselflies invaded vernal ponds

We know little about the macroevolution of life-history traits along environmental gradients, especially with regard to the directionality compared to the ancestral states and the associated costs to other functions. Here we examine how age and size at maturity evolved when Lestes damselflies shifted from their ancestral temporary pond habitat (i.e., ponds that may dry once every decade or so) to extremely ephemeral vernal ponds (ponds that routinely dry completely each year). Larvae of three species were reared from eggs until emergence under different levels of photoperiod and transient starvation stress. Compared to the two temporary-pond Lestes, the phylogenetically derived vernal-pond Lestes dryas developed more rapidly across photoperiod treatments until the final instar, and only expressed plasticity in development time in the final instar under photoperiod levels that simulated a later hatching date. The documented change in development rate can be considered adaptive and underlies the success of the derived species in vernal ponds. Results suggest associated costs of faster development are lower mass at maturity and lower immune function after transient starvation stress. These costs may not only have impeded further evolution of the routine development rate to what is physiologically maximal, but also maintained some degree of plasticity to time constraints when the habitat shift occurred.     

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

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

Maladaptive behavior reinforces a recruitment bottleneck in newly settled fishes

Settlement from the plankton ends the major dispersive stage of life for many marine organisms and exposes them to intense predation pressure in juvenile habitats. This predation mortality represents a life-history bottleneck that can determine recruitment success. At the level of individual predator–prey interactions, prey survival depends upon behavior, specifically how behavior affects prey conspicuousness and evasive ability. We conducted an experiment to identify behavioral traits and performance levels that are important determinants of which individuals survive or die soon after settlement. We measured a suite of behavioral traits on late stage, pre-settlement Ward's damsel (Pomacentrus wardi) collected using light traps. These behavioral traits included two measures of routine swimming (indicators of conspicuousness) and eight measures of escape performance to a visual startle stimulus. Fish were then released onto individual patch reefs, where divers measured an additional behavioral trait (boldness). We censused each patch reef until approximately 50% of the fish were missing (~24 h), which we assumed to be a result of predation. We used classification tree analysis to discriminate survivors from fish presumed dead based on poor behavioral performance. The classification tree revealed that individuals displaying the maladaptive combination of low escape response speed, low boldness on the reef, and high routine swimming speed were highly susceptible to predation (92.4% with this combination died within 24 h). This accounted for 55.2% of all fish that died. Several combinations of behavioral traits predicted likely survival over 24 h, but there was greater uncertainty about that prediction than there was for fish that were predicted to die. Thus maladaptive behavioral traits were easier to identify than adaptive traits.     

Sex and the Syndrome: Individual and Population Consistency in Behaviour in Rock Pool Prawn Palaemon elegans

Animal personality has been widely documented across a range of species. The concept of personality is composed of individual behavioural consistency across time and between situations, and also behavioural trait correlations known as behavioural syndromes. Whilst many studies have now investigated the stability of individual personality traits, few have analysed the stability over time of entire behavioural syndromes. Here we present data from a behavioural study of rock pool prawns. We show that prawns are temporally consistent in a range of behaviours, including activity, exploration and boldness, and also that a behavioural syndrome is evident in this population. We find correlations between many behavioural traits (activity, boldness, shoaling and exploration). In addition, behavioural syndrome structure was consistent over time. Finally, few studies have explicitly studied the role of sex differences in personality traits, behavioural consistency and syndrome structure. We report behavioural differences between male and female prawns but no differences in patterns of consistency. Our study adds to the growing literature on animal personality, and provides evidence showing that syndromes themselves can exhibit temporal consistency.     

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.     

Fitness consequences of larval traits persist across the metamorphic boundary

Metamorphosis is thought to provide an adaptive decoupling between traits specialized for each life-history stage in species with complex life cycles. However, an increasing number of studies are finding that larval traits can carry-over to influence postmetamorphic performance, suggesting that these life-history stages may not be free to evolve independently of each other. We used a phenotypic selection framework to compare the relative and interactive effects of larval size, time to hatching, and time to settlement on postmetamorphic survival and growth in a marine invertebrate, Styela plicata. Time to hatching was the only larval trait found to be under directional selection, individuals that took more time to hatch into larvae survived better after metamorphosis but grew more slowly. Nonlinear selection was found to act on multivariate trait combinations, once again acting in opposite directions for selection acting via survival and growth. Individuals with above average values of larval traits were most likely to survive, but surviving individuals with intermediate larval traits grew to the largest size. These results demonstrate that larval traits can have multiple, complex fitness consequences that persist across the metamorphic boundary; and thus postmetamorphic selection pressures may constrain the evolution of larval traits.     

Size‐induced phenotypic reaction norms in a parasitoid wasp: an examination of life‐history and behavioural traits

The amount of resources available during development often affects body size, causing phenotypic variation in life‐history traits and reproductive behaviours. However, past studies have seldom examined the reaction norms of both life‐history and behavioural traits versus body size. We measured the phenotypic plasticity of several life‐history (age‐specific egg load, egg size, longevity) and behavioural (oviposition rate, host marking rate, walking speed) traits of the egg parasitoid Telenomus podisi Ashmead (Hymenoptera: Scelionidae) in response to body size variation. We predicted that life‐history traits would show more evidence of size compensation than behavioural traits, resulting in fewer positively‐sloped size versus trait reaction norms among the former. As predicted by life‐history models, smaller wasps appear to shift resource allocation towards early‐life reproduction, having a similar egg load to large individuals 9 days after emergence. Surprisingly, longevity was unaffected by body size. However, egg size, the number of offspring produced during oviposition bouts, and the rate of subsequent egg synthesis were greater for larger individuals. In addition, as predicted, the reaction norms of behavioural traits versus body size were all positively sloped. Thus, despite possible adaptive compensatory plasticity of life‐history traits by small individuals, behavioural constraints directly related to body size would contribute to maintaining a positive size–fitness relationship.     

Genetic coordination of demography and phenology in the pitcher-plant mosquito,Wyeomyia smithii

Demographic and phenological traits compose the basic elements of an insect's life-history strategy in a seasonal environment. An insect's long-term fitness depends on its ability to exploit favorable conditions, to avoid unfavorable conditions, and to convert from one life style to the other. For the pitcher-plant mosquito, Wyeomyia smithii, we show that genetic variation exists in both development time (a demographic trait) and critical photoperiod (a phenological trait) in six populations spanning much of the species' geographical range. During the northward range expansion of W. smithii in North America, these traits have evolved independently under strong directional and stabilizing selection. The correlated response in critical photoperiod to divergent selection on development time reveals significantly positive genetic correlations in five populations and a negative correlation in one population. The positive correlations form a genetically coordinated phenotype: faster developing individuals use a shorter photoperiodic switch point and are able to exploit the late favorable season; slower developing individuals use a longer photoperiodic switch point and are able to avoid extending development into the unfavorable season. This genetic coordination of demography and phenology has not, however, prevented their independent evolution. We propose that evolutionary flexibility in W. smithii may arise in part from the reorganization of their genetic architecture following repeated founder events during their northward invasion of North America.     

Aggressiveness,Boldness and Parental Food Provisioning in Male House Wrens (Troglodytes aedon)

Behavioural syndromes have been identified in a large number of species, yet our understanding of them in an ecological context remains poor. Specifically, there are few data that relate behavioural syndromes to other biologically important behaviours and, ultimately, to reproductive success. In this field study, we examined the aggressiveness and boldness of free‐living male house wrens (Troglodytes aedon) and found a statistically significant positive relationship between these two behaviours (i.e. a behavioural syndrome). When we examined the two axes of this behavioural syndrome in relation to the male's share of provisioning, we found a negative relation between a male's aggressiveness and his provisioning rate, but no relationship between male boldness and provisioning behaviour. These differences in provisioning behaviour among males with different levels of aggression may reflect differences in reproductive strategies or different life‐history trade‐offs among males. Moreover, these results indicate that while some behavioural traits may be correlated, this does not mean that traits that compose the behavioural syndrome cannot evolve independently of one another.     

ON THE LOW HERITABILITY OF LIFE-HISTORY TRAITS

Life-history traits such as longevity and fecundity often show low heritability. This is usually interpreted in terms of Fisher's fundamental theorem to mean that populations are near evolutionary equilibrium and genetic variance in total fitness is low. We develop the causal relationship between metric traits and life-history traits to show that a life-history trait is expected to have a low heritability whether or not the population is at equilibrium. This is because it is subject to all the environmental variation in the metric traits that affect it plus additional environmental variation. There is no simple prediction regarding levels of additive genetic variance in life-history traits, which may be high at equilibrium. Several other patterns in the inheritance of life-history traits are readily predicted from the causal model. These include the strength of genetic correlations between life-history traits, levels of nonadditive genetic variance, and the inevitability of genotype-environment interaction.     

Photoperiod affects compensating developmental rate across latitudes in the damselfly Lestes sponsa

1. Although there is a great deal of theoretical and empirical data about the life history responses of time constraints in organisms, little is known about the latitude‐compensating mechanism that enables northern populations' developmental rates to compensate for latitude. To investigate the importance of photoperiod on development, offspring of the obligatory univoltine damselfly Lestes sponsa from two populations at different latitudes (53°N and 63°N) were raised in a common laboratory environment at both northern and southern photoperiods that corresponded to the sites of collection. 2. Egg development time was shorter under northern photoperiod regimes for both populations. However, the northern latitude population showed a higher phenotypic plasticity response to photoperiod compared with the southern latitude population, suggesting a genetic difference in egg development time in response to photoperiod. 3. Larvae from both latitudes expressed shorter larval development time and faster growth rates under northern photoperiod regimes. There was no difference in phenotypic plastic response between northern and southern latitude populations with regard to development time. 4. Data on field collected adults showed that adult sizes decreased with an increase in latitude. This adult size difference was a genetically fixed trait, as the same size difference between populations was also found when larvae were reared in the laboratory. 5. The results suggest phenotypic plasticity responses in life history traits to photoperiod, but also genetic differences between north and south latitude populations in response to photoperiod, which indicates the presence of a latitudinal compensating mechanism that is triggered by a photoperiod.