Elevational trends in life histories: revising the pace‐of‐life framework

Life‐history traits in birds, such as lifespan, age at maturity, and rate of reproduction, vary across environments and in combinations imposed by trade‐offs and limitations of physiological mechanisms. A plethora of studies have described the diversity of traits and hypothesized selection pressures shaping components of the survival–reproduction trade‐off. Life‐history variation appears to fall along a slow–fast continuum, with slow pace characterized by higher investment in survival over reproduction and fast pace characterized by higher investment in reproduction over survival. The Pace‐of‐Life Syndrome (POLS) is a framework to describe the slow–fast axis of variation in life‐history traits and physiological traits. The POLS corresponds to latitudinal gradients, with tropical birds exhibiting a slow pace of life. We examined four possible ways that the traits of high‐elevation birds might correspond to the POLS continuum: (i) rapid pace, (ii) tropical slow pace, (iii) novel elevational pace, or (iv) constrained pace. Recent studies reveal that birds breeding at high elevations in temperate zones exhibit a combination of traits creating a unique elevational pace of life with a central trade‐off similar to a slow pace but physiological trade‐offs more similar to a fast pace. A paucity of studies prevents consideration of the possibility of a constrained pace of life. We propose extending the POLS framework to include trait variation of elevational clines to help to investigate complexity in global geographic patterns.     

Life‐history evolution under fluctuating density‐dependent selection and the adaptive alignment of pace‐of‐life syndromes

We present a novel perspective on life‐history evolution that combines recent theoretical advances in fluctuating density‐dependent selection with the notion of pace‐of‐life syndromes (POLSs) in behavioural ecology. These ideas posit phenotypic co‐variation in life‐history, physiological, morphological and behavioural traits as a continuum from the highly fecund, short‐lived, bold, aggressive and highly dispersive ‘fast’ types at one end of the POLS to the less fecund, long‐lived, cautious, shy, plastic and socially responsive ‘slow’ types at the other. We propose that such variation in life histories and the associated individual differences in behaviour can be explained through their eco‐evolutionary dynamics with population density – a single and ubiquitous selective factor that is present in all biological systems. Contrasting regimes of environmental stochasticity are expected to affect population density in time and space and create differing patterns of fluctuating density‐dependent selection, which generates variation in fast versus slow life histories within and among populations. We therefore predict that a major axis of phenotypic co‐variation in life‐history, physiological, morphological and behavioural traits (i.e. the POLS) should align with these stochastic fluctuations in the multivariate fitness landscape created by variation in density‐dependent selection. Phenotypic plasticity and/or genetic (co‐)variation oriented along this major POLS axis are thus expected to facilitate rapid and adaptively integrated changes in various aspects of life histories within and among populations and/or species. The fluctuating density‐dependent selection POLS framework presented here therefore provides a series of clear testable predictions, the investigation of which should further our fundamental understanding of life‐history evolution and thus our ability to predict natural population dynamics.     

Behavioural Flexibility and Personality in Zebra Finches

Consistent individual differences in behaviour of animals, that is, personalities, are both widespread and widely studied, but very few studies also include cognitive traits in this context. Animal personality has recently been integrated into the pace‐of‐life‐syndrome hypothesis, relating individual behavioural traits to life history. Variation in cognitive traits could be explained well by this theoretical framework. A risk‐reward trade‐off might lead to different cognitive types: Active birds that learn fast, take risks and probably have a fast lifestyle and less active, slow learning birds that are risk averse but thereby perform better in reversal learning as they probably pay more attention to external cues. We investigated the performance of zebra finches (Taeniopygia guttata) in a cognitively challenging reversal learning task and linked this to two personality traits: activity and fearfulness. Male birds were better in reversal learning than females. While no personality‐related differences occurred in the initial learning of our task, more active and fearful birds relearned the cue–reward association faster. While birds of different sex might have revealed different risk‐taking strategies in the training, our findings do not reveal the expected direction of a risk‐reward trade‐off in the reversal learning. It seems likely that a more general and personality‐related cognitive ability might improve performance across different tasks. The linkage between personality and cognition documented here could hence suggest that cognitive traits are indeed part of an overall pace‐of‐life syndrome.     

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.     

Autistic-like and schizotypal traits in a life history perspective: diametrical associations with impulsivity,sensation seeking,and sociosexual behavior

According to recent theoretical models, autistic-like and schizotypal traits can be regarded as opposite sides of a single continuum of variation in personality and cognition, and may be diametrically associated with individual differences in life history strategies. In this view, schizotypy is a psychological phenotype oriented toward high mating effort and reduced parenting, consistent with a fast life history strategy, whereas autistic-like traits contribute to a slow strategy characterized by reduced mating effort and high parental investment. In this study, we tested the hypothesis that autistic-like and schizotypal traits would be diametrically associated with unrestricted sociosexuality, impulsivity, and sensation seeking (three key behavioral correlates of fast life history strategies in humans) in a sample of 152 young adults (18–38 years). The results were consistent with a diametrical autism–schizotypy axis of individual variation. In line with our hypotheses, autism–schizotypy scores were uniquely associated with individual differences in impulsivity, sensation seeking, and sociosexual behavior, even after controlling for variation in Big Five personality traits. However, we found no significant associations with sociosexual attitude in the present sample. Our findings provide additional support for a life history model of autistic-like and schizotypal traits and demonstrate the heuristic value of this approach in the study of personality and psychopathology.     

Repeatability and correlation of physiological traits: Do ectotherms have a “thermal type”?

Across a range of taxa, individuals within a species differ in suites of correlated traits. These trait complexes, known as syndromes, can have dramatic evolutionary consequences as they do not evolve independently but rather as a unit. Current research focuses primarily on syndromes relating to aspects of behavior and life history. What is less clear is whether physiological traits also form a syndrome. We measured 10 thermal traits in the delicate skink, Lampropholis delicata, to test this idea. Repeatability was calculated and their across‐context correlations evaluated. Our results were in alignment with our predictions in that individual thermal traits varied consistently and were structured into a physiological syndrome, which we are referring to as the thermal behavior syndrome (TBS). Within this syndrome, lizards exhibited a “thermal type” with each being ranked along a cold–hot continuum. Hot types had faster sprint speeds and higher preferred body temperatures, whereas the opposite was true for cold types. We conclude that physiological traits may evolve as a single unit driven by the need to maintain optimal temperatures that enable fitness‐related behaviors to be maximized.     

Explorative behaviour is not associated with metabolism in the European Pied Flycatcher Ficedula hypoleuca

The pace‐of‐life syndrome hypothesis (POLS) represents an attractive theoretical framework suggesting that physiological and behavioural traits have evolved together with environmental conditions and life‐history strategies. POLS predicts that metabolic differences covary with behavioural variation such that high metabolic rate is associated with risk‐prone behaviour and a faster pace‐of‐life, whereas a low metabolic rate is associated with risk‐averse behaviour and a slower pace‐of‐life. We tested the POLS hypothesis in captive European Pied Flycatchers during their first year by examining the relationship between explorative behaviour and basal metabolic rate. Our results are inconsistent with POLS. The positive association of explorative behaviour with basal metabolic rate was not recovered for either sex, possibly due to foraging conditions in the aviaries where control and trial groups were fed twice a day, the birds' young age, developmental plasticity, or a non‐existent syndrome.     

A review of urban impacts on avian life‐history evolution: Does city living lead to slower pace of life?

The concept of a pace‐of‐life syndrome describes inter‐ and intraspecific variation in several life‐history traits along a slow‐to‐fast pace‐of‐life continuum, with long lifespans, low reproductive and metabolic rates, and elevated somatic defences at the slow end of the continuum and the opposite traits at the fast end. Pace‐of‐life can vary in relation to local environmental conditions (e.g. latitude, altitude), and here we propose that this variation may also occur along an anthropogenically modified environmental gradient. Based on a body of literature supporting the idea that city birds have longer lifespans, we predict that urban birds have a slower pace‐of‐life compared to rural birds and thus invest more in self maintenance and less in annual reproduction. Our statistical meta‐analysis of two key traits related to pace‐of‐life, survival and breeding investment (clutch size), indicated that urban birds generally have higher survival, but smaller clutch sizes. The latter finding (smaller clutches in urban habitats) seemed to be mainly a characteristic of smaller passerines. We also reviewed urbanization studies on other traits that can be associated with pace‐of‐life and are related to either reproductive investment or self‐maintenance. Though sample sizes were generally too small to conduct formal meta‐analyses, published literature suggests that urban birds tend to produce lower‐quality sexual signals and invest more in offspring care. The latter finding is in agreement with the adult survival hypothesis, proposing that higher adult survival prospects favour investment in fewer offspring per year. According to our hypothesis, differences in age structure should arise between urban and rural populations, providing a novel alternative explanation for physiological differences and earlier breeding. We encourage more research investigating how telomere dynamics, immune defences, antioxidants and oxidative damage in different tissues vary along the urbanization gradient, and suggest that applying pace‐of‐life framework to studies of variation in physiological traits along the urbanization gradient might be the next direction to improve our understanding of urbanization as an evolutionary process.     

Herpetological diversity along Andean elevational gradients: links with physiological ecology and evolutionary physiology

A well-defined macroecological pattern is the decline in biodiversity with altitude. However, this decline is taxa-specific. For example, amphibians are more diverse than squamates at extreme elevations in the tropical Andes, but this pattern is reversed at extreme elevations in the southern latitudes. Several ecophysiological and evolutionary factors may be related to this difference. At high-elevations in southern latitudes temperature differs dramatically among seasons and dry soils dominate, characteristics that appear to favor lizard physiological ecology. Tropical high altitudes, in contrast, are humid and offer abundant and diverse water resources. These characteristics allow for a richer anuran community but might complicate lizard egg development through temperature and oxygen constrains. Differences in strategies of thermal adaptation might also modulate diversity patterns. The thermal physiology of anurans is extremely labile so that behavioral and physiological performance is maintained despite an altitudinal decrease in field body temperature. Lizards, in contrast, exhibit a conservative thermal physiology and rely on behavioral thermoregulation to face cold and variable temperatures. Both, lizard behavioral strategies and anuran physiological adjustments seem equally efficient in allowing ecological success and diversification for both groups in the tropics up to approximately 3000 m. At higher elevations physiological thermal adaptation is required, and lizards are ecologically constrained, perhaps at various ontogenetic stages. Patterns of biodiversity along environmental clines can be better understood through a physiological approach, and can help to refine and propose hypotheses in evolutionary physiology.     

Behavioral drive versus behavioral inertia in evolution: a null model approach

Some biologists embrace the classical view that changes in behavior inevitably initiate or drive evolutionary changes in other traits, yet others note that behavior sometimes inhibits evolutionary changes. Here we develop a null model that quantifies the impact of regulatory behaviors (specifically, thermoregulatory behaviors) on body temperature and on performance of ectotherms. We apply the model to data on a lizard (Anolis cristatellus) and show that thermoregulatory behaviors likely inhibit selection for evolutionary shifts in thermal physiology with altitude. Because behavioral adjustments are commonly used by ectotherms to regulate physiological performance, regulatory behaviors should generally constrain rather than drive evolution, a phenomenon we call the "Bogert effect." We briefly review a few other examples that contradict the classical view of behavior as the inevitable driving force in evolution. Overall, our analysis and brief review challenge the classical view that behavior is invariably the driving force in evolution, and instead our work supports the alternative view that behavior has diverse--and sometimes conflicting--effects on the directions and rates at which other traits evolve.     

Problem‐solving skills are linked to parental care and offspring survival in wild house sparrows

Individuals within a population often exhibit consistent differences in important behavioral traits such as parental care. One interesting, yet largely unexplored explanation for the existence of these consistent differences among parents is the idea that cognitive differences between individuals could lead to between‐individual variation in parenting behavior. I used a wild population of house sparrows (Passer domesticus) to test the nature of the relationship between aspects of cognitive ability (problem‐solving performance and learning) and parental care behavior, both measured in the wild. Furthermore, because parental care is tightly linked to fitness, I also investigated the relationship between problem‐solving performance and offspring survival. Parent sparrows were presented with a novel problem‐solving task that required them to remove an obstacle to obtain food. While there was no relationship between the ability to complete the task and measures of parental care (nestling provisioning rate or likelihood of provisioning with large food items), parents that solved the task quickly had higher provisioning rates than slow solvers. Additionally, the ability of fathers to complete the problem‐solving task was positively related to offspring survival. These results provide evidence that aspects of problem‐solving performance are positively correlated with parenting behavior and fitness in the wild.     

Age at the onset of senescence in birds and mammals is predicted by early-life performance

Life-history theory predicts that traits involved in maturity, reproduction and survival correlate along a fast–slow continuum of life histories. Evolutionary theories and empirical results indicate that senescence-related traits vary along this continuum, with slow species senescing later and at a slower pace than fast species. Because senescence patterns are typically difficult to estimate from studies in the wild, here we propose to predict the associated trait values in the frame of life-history theory. From a comparative analysis based on 81 free-ranging populations of 72 species of birds and mammals, we find that a nonlinear combination of fecundity, age at first reproduction and survival over the immature stage can account for ca two-thirds of the variance in the age at the onset of actuarial senescence. Our life-history model performs better than a model predicting the onset based on generation time, and it only includes life-history traits during early life as explanatory variables, i.e. parameters that are both theoretically expected to shape senescence and are measurable within relatively short studies. We discuss the good-fit of our life-history model to the available data in the light of current evolutionary theories of senescence. We further use it to evaluate whether studies that provided no evidence for senescence lasted long enough to include the onset of senescence.     

Beyond spider personality: The relationships between behavioral,physiological, and environmental factors

Spiders are useful models for testing different hypotheses and methodologies relating to animal personality and behavioral syndromes because they show a range of behavioral types and unique physiological traits (e.g., silk and venom) that are not observed in many other animals. These characteristics allow for a unique understanding of how physiology, behavioral plasticity, and personality interact across different contexts to affect spider''s individual fitness and survival. However, the relative effect of extrinsic factors on physiological traits (silk, venom, and neurohormones) that play an important role in spider survival, and which may impact personality, has received less attention. The goal of this review is to explore how the environment, experience, ontogeny, and physiology interact to affect spider personality types across different contexts. We highlight physiological traits, such as neurohormones, and unique spider biochemical weapons, namely silks and venoms, to explore how the use of these traits might, or might not, be constrained or limited by particular behavioral types. We argue that, to develop a comprehensive understanding of the flexibility and persistence of specific behavioral types in spiders, it is necessary to incorporate these underlying mechanisms into a synthesized whole, alongside other extrinsic and intrinsic factors.     

On the evolution of personalities via frequency-dependent selection

Personality differences can be found in a wide range of species across the animal kingdom, but why natural selection gave rise to such differences remains an open question. Frequency-dependent selection is a potent mechanism explaining variation; it does not explain, however, the other two key features associated with personalities, consistency and correlations. Using the hawk-dove game and a frequency-dependent foraging game as examples, we here show that this changes fundamentally whenever one takes into account the physiological architecture underlying behavior (e.g., metabolism). We find that the inclusion of physiology changes the evolutionary predictions concerning consistency and correlations: while selection gives rise to inconsistent individuals and stochastically fluctuating behavioral correlations in scenarios that neglect physiology, we find high levels of behavioral consistency and tight and stable trait correlations in scenarios that incorporate physiology. The coevolution of behavioral and physiological traits also gives rise to adaptive physiological differences that are systematically associated with behavioral differences. As well as providing a framework for understanding behavioral consistency and behavioral correlations, our work thus also provides an explanation for systematic physiological differences within populations, a phenomenon that appears to exist in a wide range of species but that, up to now, has been poorly understood.     

Ecological frames of mind: the role of cognition in behavioral ecology.

Cognitive psychology is the study of how information, from the senses and from memory, is used in the production of behavior. Investigation of the specifics of behavioral adaptation has already led some behavioral ecologists into the domain of animal cognition. I make several arguments for the benefits and the necessity of a sophisticated assessment by ecologists of the cognitive aspects of behavioral adaptation. First, because cognition typically serves to produce adaptive behavior, cognitive structure and function should reflect ecological demands; studies of cognition in ecological contexts are opportunities to understand adaptation. Furthermore, constraints on cognitive properties may help determine how behavior meets the environment. Studies of spatial memory in food-caching corvids exemplify how cognitive aspects of behavior may both reflect and determine specifics of adaptation. Second, many models in behavioral ecology assume certain cognitive abilities, such as timing or counting. Cognitive theory and methodology should be used to determine whether animals possess these abilities. I have provided examples. Third, consideration of cognitive function can lead to original ideas about the details of behavioral adaptation. Without a thorough integration of cognitive psychology with behavioral ecology, our understanding of the relation between behavior and selective pressures will be compromised.     

Simulated heat waves reduce cognitive and motor performance of an endotherm

1. Heat waves cause mass mortality of animals, including humans, across the globe annually, which has drawn new attention to how animals cope with high air temperatures. Recent field research has explored behavioral responses to high air temperatures, which can influence reproductive success and mortality.
2. Less well studied are the effects of high air temperatures on cognition, which may underlie behavioral changes. Specifically, it is poorly known if cognitive declines occur at high temperatures, and if cognitive and motor components of behavior are similarly affected.
3. We tested how well zebra finches (Taeniopygia guttata castanotis), a model for cognition research, performed two learned foraging tasks (color association and detour‐reaching) at mild (22°C) and high (43 and 44°C) air temperatures that occur naturally in their range. We habituated birds to the trial conditions and temperatures on days preceding the test trials and at the trial temperature for 30 min immediately prior to each test trial. Trials lasted less than 10 min. At high air temperatures, zebra finches exhibited heat dissipation behaviors during most tasks, suggesting thermoregulatory challenge.
4. Cognitive performance declined at high air temperatures in two of three measures: Color association was unaffected, but birds missed more food rewards, and did more unproductive behaviors. Motor performance declined at high temperatures on the color association task, including longer times to complete the task, move between food rewards, and process individual seeds. Performance declines varied among components of behavior and among individuals.
5. We combined our behavioral data with existing climate data and predicted that in the austral summer of 2018–2019, zebra finches experienced air temperatures that caused cognitive and motor declines in our captive birds in 34% and 45% of their Australian range, respectively.
6. This study provides novel experimental evidence that high air temperatures cause cognitive and motor performance decline in birds. Further, our results provide insights to how those declines might affect bird ecology and evolution. First, differences in declines among behavioral components may allow identification of behaviors that are most susceptible to decline in the wild. Second, variation in performance declines and heat dissipation behaviors among individuals suggests variability in heat tolerance, which could lead to differential fitness in the wild. Last, these results suggest that high air temperatures cause cognitive declines in the wild and that understanding cognition could help refine predictive models of population persistence.

     

Elucidating Poor Decision-Making in a Rat Gambling Task

Although poor decision-making is a hallmark of psychiatric conditions such as attention deficit/hyperactivity disorder, pathological gambling or substance abuse, a fraction of healthy individuals exhibit similar poor decision-making performances in everyday life and specific laboratory tasks such as the Iowa Gambling Task. These particular individuals may provide information on risk factors or common endophenotypes of these mental disorders. In a rodent version of the Iowa gambling task – the Rat Gambling Task (RGT), we identified a population of poor decision makers, and assessed how these rats scored for several behavioral traits relevant to executive disorders: risk taking, reward seeking, behavioral inflexibility, and several aspects of impulsivity. First, we found that poor decision-making could not be well predicted by single behavioral and cognitive characteristics when considered separately. By contrast, a combination of independent traits in the same individual, namely risk taking, reward seeking, behavioral inflexibility, as well as motor impulsivity, was highly predictive of poor decision-making. Second, using a reinforcement-learning model of the RGT, we confirmed that only the combination of extreme scores on these traits could induce maladaptive decision-making. Third, the model suggested that a combination of these behavioral traits results in an inaccurate representation of rewards and penalties and inefficient learning of the environment. Poor decision-making appears as a consequence of the over-valuation of high-reward-high-risk options in the task. Such a specific psychological profile could greatly impair clinically healthy individuals in decision-making tasks and may predispose to mental disorders with similar symptoms.     

Linking fearfulness and coping styles in fish

Consistent individual differences in cognitive appraisal and emotional reactivity, including fearfulness, are important personality traits in humans, non-human mammals, and birds. Comparative studies on teleost fishes support the existence of coping styles and behavioral syndromes also in poikilothermic animals. The functionalist approach to emotions hold that emotions have evolved to ensure appropriate behavioral responses to dangerous or rewarding stimuli. Little information is however available on how evolutionary widespread these putative links between personality and the expression of emotional or affective states such as fear are. Here we disclose that individual variation in coping style predicts fear responses in Nile tilapia Oreochromis niloticus, using the principle of avoidance learning. Fish previously screened for coping style were given the possibility to escape a signalled aversive stimulus. Fearful individuals showed a range of typically reactive traits such as slow recovery of feed intake in a novel environment, neophobia, and high post-stress cortisol levels. Hence, emotional reactivity and appraisal would appear to be an essential component of animal personality in species distributed throughout the vertebrate subphylum.     

Research progress on Drosophila visual cognition in China

Visual cognition,as one of the fundamental aspects of cognitive neuroscience,is generally associated with high-order brain functions in animals and human.Drosophila,as a model organism,shares certain features of visual cognition in common with mammals at the genetic,molecular,cellular,and even higher behavioral levels.From learning and memory to decision making,Drosophila covers a broad spectrum of higher cognitive behaviors beyond what we had expected.Armed with powerful tools of genetic manipulation in Drosophila,an increasing number of studies have been conducted in order to elucidate the neural circuit mechanisms underlying these cognitive behaviors from a genes-brain-behavior perspective.The goal of this review is to integrate the most important studies on visual cognition in Drosophila carried out in mainland China during the last decade into a body of knowledge encompassing both the basic neural operations and circuitry of higher brain function in Drosophila.Here,we consider a series of the higher cognitive behaviors beyond learning and memory,such as visual pattern recognition,feature and context generalization,different feature memory traces,salience-based decision,attention-like behavior,and cross-modal leaning and memory.We discuss the possible general gain-gating mechanism implementing by dopamine-mushroom body circuit in fly's visual cognition.We hope that our brief review on this aspect will inspire further study on visual cognition in flies,or even beyond.     

ASYNCHRONOUS EVOLUTION OF PHYSIOLOGY AND MORPHOLOGY IN ANOLIS LIZARDS

Species‐rich adaptive radiations typically diversify along several distinct ecological axes, each characterized by morphological, physiological, and behavioral adaptations. We test here whether different types of adaptive traits share similar patterns of evolution within a radiation by investigating patterns of evolution of morphological traits associated with microhabitat specialization and of physiological traits associated with thermal biology in Anolis lizards. Previous studies of anoles suggest that close relatives share the same “structural niche” (i.e., use the same types of perches) and are similar in body size and shape, but live in different “climatic niches” (i.e., use habitats with different insolation and temperature profiles). Because morphology is closely tied to structural niche and field active body temperatures are tied to climatic niches in Anolis, we expected phylogenetic analyses to show that morphology is more evolutionarily conservative than thermal physiology. In support of this hypothesis, we find (1) that thermal biology exhibits more divergence among recently diverged Anolis taxa than does morphology; and (2) diversification of thermal biology among all species often follows diversification in morphology. These conclusions are remarkably consistent with predictions made by anole biologists in the 1960s and 1970s.