Boldness behavior and stress physiology in a novel urban environment suggest rapid correlated evolutionary adaptation

Novel or changing environments expose animals to diverse stressors that likely require coordinated hormonal and behavioral adaptations. Predicted adaptations to urban environments include attenuated physiological responses to stressors and bolder exploratory behaviors, but few studies to date have evaluated the impact of urban life on codivergence of these hormonal and behavioral traits in natural systems. Here, we demonstrate rapid adaptive shifts in both stress physiology and correlated boldness behaviors in a songbird, the dark-eyed junco, following its colonization of a novel urban environment. We compared elevation in corticosterone (CORT) in response to handling and flight initiation distances in birds from a recently established urban population in San Diego, California to birds from a nearby wildland population in the species' ancestral montane breeding range. We also measured CORT and exploratory behavior in birds raised from early life in a captive common garden study. We found persistent population differences for both reduced CORT responses and bolder exploratory behavior in birds from the colonist population, as well as significant negative covariation between maximum CORT and exploratory behavior. Although early developmental effects cannot be ruled out, these results suggest contemporary adaptive evolution of correlated hormonal and behavioral traits associated with colonization of an urban habitat.     

Differential migration and an endocrine response to stress in wintering dark-eyed juncos (Junco hyemalis)

The dark-eyed junco (junco hyemalis) exhibits differential migration in autumn that, in general, results in females overwintering south of males, and young within each sex overwintering north of older birds. Individuals overwintering at higher latitudes face less predictable and more challenging environmental conditions. Rapid increases in circulating levels of the energy-regulating glucocorticosteroid, corticosterone, occur in response to environmental stressors. To establish whether the strength of acute corticosterone secretion was correlated with the probability of encountering poor environmental conditions, we compared the corticosterone stress response (e.g. initial plasma concentrations at the time of capture and 30 min later) in dark-eyed juncos overwintering in Mississippi (MS), USA, near the southern limit of their wintering range, with juncos overwintering in New York (NY), USA, near the northern limit of their wintering range. During two winters, 22 males and one female were sampled in NY; 13 males, 12 females and one bird of undetermined sex were sampled in MS. Not unexpectedly, NY birds carried greater fat reserves that resulted in a significantly higher value of energetic condition (mass corrected for wing cord cubed). There was no difference between the two winters sampled at either site, nor was there an effect of sex on patterns of corticosterone secretion in MS birds. With sexes pooled, MS and NY birds had similar baseline corticosterone levels. However, as predicted, NY birds exhibited significantly higher corticosterone concentrations 30 min after capture. These results support the hypothesis that birds wintering in less predictable, more extreme environments show a higher amplitude corticosterone response, which may enable them to adjust their behaviour and physiology more rapidly in response to environmental stressors such as storms. Adrenocortical sensitivity may be a part of the physiological milieu associated with differential migration in juncos; whether it results from endogenous differences in the migratory programmes of individuals or from acclimatization to local environmental conditions remains to be determined.     

Risk‐taking and the evolution of mechanisms for rapid escape from predators

Flight initiation distance (FID) is the distance at which an individual animal takes flight when approached by a human. This behavioural measure of risk‐taking reflects the risk of being captured by real predators, and it correlates with a range of life history traits, as expected if flight distance optimizes risk of predation. Given that FID provides information on risk of predation, we should expect that physiological and morphological mechanisms that facilitate flight and escape predict interspecific variation in flight distance. Haematocrit is a measure of packed red blood cell volume and as such indicates the oxygen transport ability and hence the flight muscle contracting reaction of an individual. Therefore, we predicted that species with short flight distances, that allow close proximity between a potential prey individual and a predator, would have high haematocrit. Furthermore, we predicted that species with large wing areas and hence relatively low costs of flight and species with large aspect ratios and hence high manoeuvrability would have evolved long flight speed. Consistent with these predictions, we found in a sample of 63 species of birds that species with long flight distances for their body size had low levels of haematocrit and large wing areas and aspect ratios. These findings provide evidence consistent with the evolution of risk‐taking behaviour being underpinned by physiological and morphological mechanisms that facilitate escape from predators and add to our understanding of predator–prey coevolution.     

Zebra finches are bolder in an asocial, rather than social, context

Despite an expanding interest in animal personalities, the influence of social interactions and sex differences on individual differences in behaviour remains poorly understood. Using the social zebra finch (Taeniopygia guttata), we tested for behavioural differences in exploration of a novel environment and objects, between individuals of both sexes in relation to a social context; the presence of three male companions, three female companions or no companion birds. We predicted that the presence of conspecific companions should result in focal birds reacting to novelty by exploring more extensively because the companion birds contribute to anti-predator vigilance behaviour and because social isolation often causes behavioural inhibition in social species. We found that exploratory behaviour of focal individuals was significantly reduced in the presence of conspecific companions, irrespective of the companion's sex. Moreover, we found a weak trend towards females being more exploratory than males, irrespective of the social context. These results demonstrate the importance of considering the social context in animal personality studies and of exploring sex differences in personalities.     

Developmental stress can uncouple relationships between physiology and behaviour

Phenotypic correlations (r_P) have frequently been observed between physiological and behavioural traits, and the nature of these associations has been shown to be modulated by a range of environmental stressors. Studies to date have examined the effects of acute stressors on physiology–behaviour interrelations, but the potential for permanent changes induced by exposure to stress during development remains unexplored. We exposed female zebra finches to dietary restriction during the nestling stage and tested how this affected r_P among a variety of physiological traits (haematocrit, stress-induced corticosterone level and basal metabolic rate (BMR)) and behavioural traits (activity and feeding rates in novel and familiar environments). Developmental stress completely uncoupled the relationship between activity in a novel environment and two physiological traits: haematocrit and BMR. This suggests that nutritionally based developmental stress has provoked changes in the energy budget that alleviate the trade-off between maintenance (BMR) and locomotor activities.     

Successful despite poor flight performance: range expansion is associated with enhanced exploratory behaviour and fast development

Anthropogenic interference forces species to respond to changing environmental conditions. One possible response is dispersal and concomitant range shifts, allowing individuals to escape unfavourable conditions or to track the shifting climate niche. Range expansions depend on both dispersal capacity and the ability to establish populations beyond the former range. We here compare well‐established core populations with recently established edge populations in the currently northward expanding butterfly Lycaena tityrus. Edge populations were characterized by shorter development times and smaller size, a higher sensitivity to high temperature and an enhanced exploratory behaviour. The differences between core and edge populations found suggest adaptation to local climates and an enhanced dispersal ability in edge populations. In particular, enhanced exploratory behaviour may be advantageous in all steps of the dispersal process and may have facilitated the current range expansion. This study describes differences associated with a current range expansion, knowledge which might be useful for a better understanding of species responses to environmental change. We further report on variation between males and females in morphology and flight behaviour, with males showing a longer flight endurance and more pronounced exploratory behaviour than females.     

Genetics of behavioural adaptation of livestock to farming conditions

Behavioural adaptation of farm animals to environmental changes contributes to high levels of production under a wide range of farming conditions, from highly controlled indoor systems to harsh outdoor systems. The genetic variation in livestock behaviour is considerable. Animals and genotypes with a larger behavioural capacity for adaptation may cope more readily with varying farming conditions than those with a lower capacity for adaptation. This capacity should be exploited when the aim is to use a limited number of species extensively across the world. The genetics of behavioural traits is understood to some extent, but it is seldom accounted for in breeding programmes. This review summarizes the estimates of genetic parameters for behavioural traits in cattle, pigs, poultry and fish. On the basis of the major studies performed in the last two decades, we focus the review on traits of common interest in the four species. These concern the behavioural responses to both acute and chronic stressors in the physical environment (feed, temperature, etc.) and those in the social environment (other group members, progeny, humans). The genetic strategies used to improve the behavioural capacity for adaptation of animals differ between species. There is a greater emphasis on responses to acute environmental stress in fish and birds, and on responses to chronic social stress in mammals.     

Corticosterone,testosterone and life-history strategies of birds

Steroid hormones have similar functions across vertebrates, but circulating concentrations can vary dramatically among species. We examined the hypothesis that variation in titres of corticosterone (Cort) and testosterone (T) is related to life-history traits of avian species. We predicted that Cort would reach higher levels under stress in species with higher annual adult survival rates since Cort is thought to promote physiological and behavioural responses that reduce risk to the individual. Conversely, we predicted that peak T during the breeding season would be higher in short-lived species with high mating effort as this hormone is known to promote male fecundity traits. We quantified circulating hormone concentrations and key life-history traits (annual adult survival rate, breeding season length, body mass) in males of free-living bird species during the breeding season at a temperate site (northern USA) and a tropical site (central Panama). We analysed our original data by themselves, and also combined with published data on passerine birds to enhance sample size. In both approaches, variation in baseline Cort (Cort0) among species was inversely related to breeding season length and body mass. Stress-induced corticosterone (MaxCort) also varied inversely with body mass and, as predicted, also varied positively with annual adult survival rates. Furthermore, species from drier and colder environments exhibited lower MaxCort than mesic and tropical species; T was lowest in species from tropical environments. These findings suggest that Cort0, MaxCort and T modulate key vertebrate life-history responses to the environment, with Cort0 supporting energetically demanding processes, MaxCort promoting survival and T being related to mating success.     

Expanding population edges: theories,traits, and trade‐offs

Recent patterns of global change have highlighted the importance of understanding the dynamics and mechanisms of species range shifts and expansions. Unique demographic features, spatial processes, and selective pressures can result in the accumulation and evolution of distinctive phenotypic traits at the leading edges of expansions. We review the characteristics of expanding range margins and highlight possible mechanisms for the appearance of phenotypic differences between individuals at the leading edge and core of the range. The development of life history traits that increase dispersal or reproductive ability is predicted by theory and supported with extensive empirical evidence. Many examples of rapid phenotypic change are associated with trade‐offs that may influence the persistence of the trait once expansion ends. Accounting for the effects of edge phenotypes and related trade‐offs could be critical for predicting the spread of invasive species and population responses to climate change.     

Speed of exploration and risk-taking behavior are linked to corticosterone titres in zebra finches

The existence of consistent individual differences in behavioral strategies ("personalities" or coping styles) has been reported in several animal species. Recent work in great tits has shown that such traits are heritable and exhibit significant genetic variation. Free-living birds respond to environmental stresses by up-regulating corticosterone production. Behavior during mild stress can occur in accordance to two types of coping styles, i.e. active and passive. Using artificially selected lines of zebra finches that vary in the amount of corticosterone produced in response to a manual restraint stressor we ran three "personality" experiments. We show that birds in the different corticosterone lines differ in their exploratory and risk-taking behaviors. There was an increase in exploratory behavior as corticosterone titre increased but only in the low corticosterone line. Birds in high corticosterone line showed greater risk-taking behavior than birds in the other lines. Thus, in general, higher levels of circulating corticosterone following a mild stress result in greater exploratory behavior and greater risk taking. This study shows that lines of animals selected for endocrine hormonal responses differ in their "coping" styles or "personalities".     

Population differentiation and behavioural association of the two ‘personality’ genes DRD4 and SERT in dunnocks (Prunella modularis)

Quantifying the variation in behaviour‐related genes within and between populations provides insight into how evolutionary processes shape consistent behavioural traits (i.e. personality). Deliberate introductions of non‐native species offer opportunities to investigate how such genes differ between native and introduced populations and how polymorphisms in the genes are related to variation in behaviour. Here, we compared the genetic variation of the two ‘personality’ genes, DRD4 and SERT, between a native (United Kingdom, UK) and an introduced (New Zealand, NZ) population of dunnocks, Prunella modularis. The NZ population showed a significantly lower number of single nucleotide polymorphisms (SNPs) compared to the UK population. Standardized F’_st estimates of the personality genes and neutral microsatellites indicate that selection (anthropogenic and natural) probably occurred during and post the introduction event. Notably, the largest genetic differentiation was found in the intronic regions of the genes. In the NZ population, we also examined the association between polymorphisms in DRD4 and SERT and two highly repeatable behavioural traits: flight‐initiation distance and mating status (promiscuous females and cobreeding males). We found 38 significant associations (for different allele effect models) between the two behavioural traits and the studied genes. Further, 22 of the tested associations showed antagonistic allele effects for males and females. Our findings illustrate how introduction events and accompanying ecological changes could influence the genetic diversity of behaviour‐related genes.     

Non-native gall-inducing insects on forest trees: a global review

Gall-inducing insects cause the development of specialised plant tissues (galls) that provide them with nutrition and some measure of protection from physical and biotic stresses. Their interaction with the plant is the most intimate metabolically of any herbivore group and is often associated with high host specificity. We survey the gall inducers that have become invasive pests of forest trees, most of which belong to just four insect families in three orders: Hemiptera (Adelgidae), Diptera (Cecidomyiidae) and Hymenoptera (Cynipidae and Eulophidae). Most are associated with introduction of plants on which they are specialists, but some have also shifted from introduced to native plant hosts. No formal comparative analysis of traits associated with success of establishment and subsequent range expansion has yet been made, and it is often hard to identify why one species has become a major range-expanding pest, while closely related and biologically very similar species have not. We provide an overview of biological traits likely to facilitate gall inducer range expansion, and highlight the importance of natural enemies in community impacts and biological control. Increasing global trade is likely to result in further range expansions by economically damaging species. The effects of climate change on the direction, frequency, and impact of gall inducer range expansions are likely to be complex and probably species-specific.     

Does short-term fasting lead to stressed-out parents? A study of incubation commitment and the hormonal stress responses and recoveries in snow petrels

The hormonal stress response is flexible and can be modulated by individuals according to its costs and benefits. Therefore, it is predicted that parents in poor body condition should modify their hormonal stress response, and thus, redirect energy allocation processes from parental care to self-maintenance when stressors occur. To test this prediction, most studies on free-living vertebrates have only focused on the stress response while the stress recovery – how quickly hormonal levels return to baseline values – has been neglected. Moreover, most studies have only focused on corticosterone – the primary mediator of allostasis – without paying attention to prolactin despite its major role in mediating parental behaviors. Here, we examined the effect of a short-term fasting event on the corticosterone and prolactin stress responses and recoveries, and we subsequently explored their relationships with parental decision in the snow petrel (Pagodroma nivea). By comparing the hormonal profiles of fasting and non-fasting snow petrels, we showed that parents modulate their corticosterone (but not prolactin) stress response according to their energetic status. We also described for the first time the hormonal stress recoveries in wild birds and found that they did not differ between fasting and non-fasting birds. Importantly, egg neglect was negatively correlated with circulating prolactin but not corticosterone levels in this species, demonstrating therefore a complex link between body condition, parental behavior and circulating corticosterone and prolactin levels. We suggest that both corticosterone and prolactin play a major role in the way parents adjust to stressors. This multiple signaling may allow parents to fine-tune their response to stressors, and especially, to activate specific allostasis-related mechanisms in a timely manner.     

Effects of corticosterone treatment on growth, development, and the corticosterone response to handling in young Japanese quail (Coturnix coturnix japonica)

Corticosterone, a glucocorticoid secreted during stress responses, has a range of actions that help birds respond to stressors. Although effects of corticosterone treatment have been described in several avian species, the impacts of defined increases in plasma corticosterone on early development and on corticosterone stress responses are little known. These issues were addressed by providing quail with different doses of corticosterone in drinking water from days 8 to 38 post-hatch. The corticosterone dose consumed by each bird during treatment days 15-30 was calculated by measuring water intake. The corticosterone dose was inversely, but weakly, correlated with weights of the bursa, thymus, spleen, liver, testes, oviduct, muscle, and body, and positively correlated with peritoneal fat deposition. When birds were divided into groups based on their corticosterone intake, weights of the spleen, thymus, bursa, muscle, testes, and oviduct were significantly reduced in birds receiving the highest doses; with the exception of muscle, similar reductions were also observed in birds receiving medium doses, and thymic growth was inhibited in birds receiving low doses. The acute corticosterone stress response was measured by handling birds for 15 min. Plasma corticosterone was transiently increased at 15 min in control birds in response to the handling stressor. Some birds consuming low doses of corticosterone had corticosterone responses similar to control birds. Initial corticosterone concentrations were elevated in birds consuming higher doses of corticosterone. Plasma corticosterone in these birds decreased from 0 to 15 min, then increased from 15 to 30 min. The initial decrease could be due to corticosterone clearance, whilst the increase could indicate that the birds had a greater response than control birds to isolation as a stressor. Corticosterone treatment may have reduced the strength of corticosterone negative feedback within the hypothalamo-pituitary-adrenal axis. The results indicate that individuals and organs differ in their sensitivity to corticosterone. Moreover, elevated plasma corticosterone may disrupt the acute corticosterone stress response, and may thus reduce the ability of birds to cope with stressors.     

Sex and migratory strategy influence corticosterone levels in winter-grown feathers,with positive breeding effects in a migratory pelagic seabird

To overcome unpredictable stressful transitory events, animals trigger an allostatic response involving the hypothalamic–pituitary–adrenal cortex. This hormonal response, which involves the release of glucocorticoids which in turn mediate between the main physiological mechanisms that regulate the energetic demands and resource allocation trade-off with behavioural responses to environmental perturbations and may ultimately lead to variation in fitness. We have used the Cory’s shearwater Calonectris borealis, a sexually dimorphic pelagic seabird with a partial migratory strategy, as a model bird species to analyse a number of traits related to the stress response. We investigated whether the activation of a stressful response, mediated by corticosterone, during the wintering period (1) correlated with the previous breeding success, (2) was affected by the migratory behaviour of male birds and (3) had consequences in the fitness of the birds. Corticosterone levels in feathers grown overwinter were analysed in 61 adult birds during three consecutive migratory periods (2009–2012) and in 14 immature birds in the wintering period 2010–2011. Moreover, the levels of corticosterone were analysed in experimental birds which were freed from their reproductive duties and compared with control birds which raised fledglings to the end of the breeding period. The results show that the levels of corticosterone were sex dependent, differed between years and were affected by the migratory strategy performed by the birds. The activation of the stressful response over the wintering period generated residual carry-over effects that positively affected the reproductive output in the subsequent breeding stage, a phenomenon previously undescribed in a long-lived pelagic seabird. Our study provides evidence that the analysis of corticosterone from feathers is a useful tool to evaluate carry-over effects in birds far away from breeding sites, opening new possibilities for future studies in this field.     

Residence time,native range size,and genome size predict naturalization among angiosperms introduced to Australia

Although critical to progress in understanding (i) if, and (ii) at what rate, introduced plants will naturalize and potentially become invasive, establishing causal links between traits and invasion success is complicated by data gaps, phylogenetic nonindependence of species, the inability to control for differences between species in residence time and propagule pressure, and covariance among traits. Here, we focus on statistical relationships between genomic factors, life history traits, native range size, and naturalization status of angiosperms introduced to Australia. In a series of analyses, we alternately investigate the role of phylogeny, incorporate introduction history, and use graphical models to explore the network of conditional probabilities linking traits and introduction history to naturalization status. Applying this ensemble of methods to the largest publicly available data set on plant introductions and their fates, we found that, overall, residence time and native range size best predicted probability of naturalization. Yet, importantly, probability of naturalization consistently increased as genome size decreased, even when the effects of shared ancestry and residence time in Australia were accounted for, and that this pattern was stronger in species without a history of cultivation, but present across annual–biennials, and herbaceous and woody perennials. Thus, despite introduction biases and indirect effects of traits via introduction history, across analyses, reduced genome size was nevertheless consistently associated with a tendency to naturalize.     

Heritability and genetic correlations of fear-related behaviour in Red Junglefowl--possible implications for early domestication

Domesticated species differ from their wild ancestors in a number of traits, generally referred to as the domesticated phenotype. Reduced fear of humans is assumed to have been an early prerequisite for the successful domestication of virtually all species. We hypothesized that fear of humans is linked to other domestication related traits. For three generations, we selected Red Junglefowl (ancestors of domestic chickens) solely on the reaction in a standardized Fear of Human-test. In this, the birds were exposed for a gradually approaching human, and their behaviour was continuously scored. This generated three groups of animals, high (H), low (L) and intermediate (I) fearful birds. The birds in each generation were additionally tested in a battery of behaviour tests, measuring aspects of fearfulness, exploration, and sociality. The results demonstrate that the variation in fear response of Red Junglefowl towards humans has a significant genetic component and is genetically correlated to behavioural responses in other contexts, of which some are associated with fearfulness and others with exploration. Hence, selection of Red Junglefowl on low fear for humans can be expected to lead to a correlated change of other behavioural traits over generations. It is therefore likely that domestication may have caused an initial suite of behavioural modifications, even without selection on anything besides tameness.     

Patterns of haemosporidian prevalence along a range expansion in introduced Kenyan house sparrows Passer domesticus

Avian haemosporidian infections (of the genera Haemoproteus, Plasmodium and Leucocytozoon) can regulate passerine populations. Thus, reduction in the number of avian haemosporidian infections in a population, for example in recently introduced hosts, may facilitate host establishment or spread (i.e. enemy release). Alternatively, colonizers could decrease competitive ability of native individuals in the novel range by increasing the prevalence of avian haemosporidians in that native passerine community (i.e. novel weapons). However, whether either or both of these phenomena will occur is difficult to predict because infection risk can be highly heterogeneous and dependent upon the interaction of biotic and abiotic factors at the microclimate level, especially because of the important role of vectors for these parasites. Here, we describe which factors best predicted avian haemosporidian prevalence in populations of house sparrows Passer domesticus introduced to Kenya. House sparrows inhabit an invasion gradient in Kenya; they were introduced via the eastern port city of Mombasa in ? 1950 and have since spread west‐ward across the country. This range expansion gave us the opportunity to examine how parasite prevalence changes over small spatiotemporal scales and what role is played by environmental and individual traits. Among all individuals, body mass was the strongest predictor of infection, with larger house sparrows being more likely to be infected. At the population level, capture month, precipitation (higher prevalence with more rainfall), and population age (increasing prevalence with increasing time since introduction) were important risk factors. Overall, haemosporidian prevalence in Kenyan house sparrows appears to be more strongly associated with individual characteristics rather than with time since introduction as was predicted, though this does not necessarily rule out a role for enemy release or novel weapons in this system.     

Personality and urbanization: behavioural traits and <Emphasis Type="Italic">DRD4</Emphasis> SNP830 polymorphisms in great tits in Barcelona city

Most examples of adaptation to the urban environment relate to plasticity processes rather than to natural selection. Personality, however, defined as consistent individual differences in behaviour related to exploration, caution, and neophobia, is a good behavioural candidate character to study natural selection in relation to the urban habitat due to its heritable variation. The aim of this paper was to analyse variation in personality by comparing urban and forest great tits Parus major using standard tests of exploratory behaviour and boldness. We studied personality in 130 wild great tits captured in Barcelona city and nearby forests and found that urban birds were more explorative and bolder towards a novel object than forest birds. Genotype frequencies of the DRD4 SNP830 polymorphism, a gene region often associated with personality variation, varied significantly between forest and urban birds. Behavioural scores, however, were not correlated with this polymorphism in our population. Exploration scores correlated to boldness for forest birds but not for urban birds. Our findings suggest that the novel selection pressures of the urban environment favour the decoupling of behavioural traits that commonly form behavioural syndromes in the wild.     

Differences in behavioural traits among native and introduced colonies of an invasive ant

Identifying the factors that promote the success of biological invasions is a key pursuit in ecology. To date, the link between animal personality and invasiveness has rarely been studied. Here, we examined in the laboratory how Argentine ant populations from the species’ native and introduced ranges differed in a suite of behaviours related to species interactions and the use of space. We found correlations among specific behavioural traits that defined an explorative-aggressive syndrome. The Main “European” supercolony (introduced range) more readily explored novel environments, displayed more aggression, detected food resources more quickly, and occupied more space than the Catalonian supercolony (introduced range) and two other Argentine supercolonies (native range). The two native supercolonies also differed in their personalities; one harbouring the less invasive personality, while the other is intermediate between the two introduced supercolonies. Therefore, instead of a binary pattern, Argentine ant supercolonies display a behavioural continuum that is independent on their geographic origin (native/introduced ranges). Our results also suggest that variability in personality traits is correlated to differences in the ecological success of Argentine ant colonies. Differences in group personalities may facilitate the persistence and invasion of animals under novel selective pressures by promoting adaptive behaviours. We stress that the concept of animal personality should be taken into account when elucidating the mechanisms of invasiveness.