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The pace-of-life syndrome (POLS) hypothesis posits that life-history characteristics, among individual differences in behavior, and physiological traits have coevolved in response to environmental conditions. This hypothesis has generated much research interest because it provides testable predictions concerning the association between the slow-fast life-history continuum and behavioral and physiological traits. Although humans are among the most well-studied species and similar concepts exist in the human literature, the POLS hypothesis has not yet been directly applied to humans. Therefore, we aimed to (i) test predicted relationships between life history, physiology, and behavior in a human population and (ii) better integrate the POLS hypothesis with other similar concepts. Using data of a representative sample of German adolescents, we extracted maturation status for girls (menarche, n = 791) and boys (voice break, n = 486), and a set of health-related risk-taking behaviors and cardiovascular parameters. Maturation status and health-related risk behavior as well as maturation status and cardiovascular physiology covaried in boys and girls. Fast maturing boys and girls had higher blood pressure and expressed more risk-taking behavior than same-aged slow maturing boys and girls, supporting general predictions of the POLS hypothesis. Only some physiological and behavioral traits were positively correlated, suggesting that behavioral and physiological traits might mediate life-history trade-offs differently. Moreover, some aspects of POLS were sex-specific. Overall, the POLS hypothesis shares many similarities with other conceptual frameworks from the human literature and these concepts should be united more thoroughly to stimulate the study of POLS in humans and other animals. Significance statement The pace-of-life syndrome (POLS) hypothesis suggests that life history, behavioral and physiological traits have coevolved in response to environmental conditions. Here, we tested this link in a representative sample of German adolescents, using data from a large health survey (the KIGGs study) containing information on individual age and state of maturity for girls and boys, and a set of health-related risk-taking behaviors and cardiovascular parameters. We found that fast maturing girls and boys had overall higher blood pressure and expressed more risk-taking behavior than same-aged slow maturing girls and boys. Only some behavioral and physiological traits were positively correlated, suggesting that behavioral and physiological traits might mediate life-history trade-offs differently and not necessarily form a syndrome. Our results demonstrate a general link between life history, physiological and behavioral traits in humans, while simultaneously highlighting a more complex and rich set of relationships, since not all relationships followed predictions by the POLS hypothesis.
Bats are important components in tropical mammal assemblages. Unravelling the mechanisms allowing multiple syntopic bat species to coexist can provide insights into community ecology. However, dietary information on component species of these assemblages is often difficult to obtain. Here we measuredstable carbon and nitrogen isotopes in hair samples clipped from the backs of 94 specimens to indirectly examine whether trophic niche differentiation and microhabitat segregation explain the coexistence of 16 bat species at Ankarana, northern Madagascar. The assemblage ranged over 4.4% in delta N-15 and was structured into two trophic levels with phytophagous Pteropodidae as primary consumers (c. 3% enriched over plants) and different insectivorous bats as secondary consumers (c. 4% enriched over primary consumers). Bat species utilizing different microhabitats formed distinct isotopic clusters (metric analyses of delta C-13-delta N-15 bi-plots), but taxa foraging in the same microhabitat did not show more pronounced trophic differentiation than those occupying different microhabitats. As revealed by multivariate analyses, no discernible feeding competition was found in the local assemblage amongst congeneric species as compared with non-congeners. In contrast to ecological niche theory, but in accordance with studies on New and Old World bat assemblages, competitive interactions appear to be relaxed at Ankarana and not a prevailing structuring force.
Foraging by consumers acts as a biotic filtering mechanism for biodiversity at the trophic level of resources. Variation in foraging behaviour has cascading effects on abundance, diversity, and functional trait composition of the community of resource species. Here we propose diversity at giving-up density (DivGUD), i.e. when foragers quit exploiting a patch, as a novel concept and simple measure quantifying cascading effects at multiple spatial scales. In experimental landscapes with an assemblage of plant seeds, patch residency of wild rodents decreased local alpha-DivGUD (via elevated mortality of species with large seeds) and regional gamma-DivGUD, while dissimilarity among patches in a landscape (beta-DivGUD) increased. By linking theories of adaptive foraging behaviour with community ecology, DivGUD allows to investigate cascading indirect predation effects, e.g. the ecology-of-fear framework, feedbacks between functional trait composition of resource species and consumer communities, and effects of inter-individual differences among foragers on the biodiversity of resource communities.
The pace-of-life syndrome (i.e., POLS) hypothesis posits that behavioral and physiological traits mediate the trade-off between current and future reproduction. This hypothesis predicts that life history, behavioral, and physiological traits will covary under clearly defined conditions. Empirical tests are equivocal and suggest that the conditions necessary for the POLS to emerge are not always met. We nuance and expand the POLS hypothesis to consider alternative relationships among behavior, physiology, and life history. These relationships will vary with the nature of predation risk, the challenges posed by resource acquisition, and the energy management strategies of organisms. We also discuss how the plastic response of behavior, physiology, and life history to changes in ecological conditions and variation in resource acquisition among individuals determine our ability to detect a fast-slow pace of life in the first place or associations among these traits. Future empirical studies will provide most insights on the coevolution among behavior, physiology, and life history by investigating these traits both at the genetic and phenotypic levels in varying types of predation regimes and levels of resource abundance.
Perceived predation risk varies in space and time creating a landscape of fear. This key feature of an animal's environment is classically studied as a species-specific property. However, individuals differ in how they solve the tradeoff between safety and reward and may, hence, differ consistently and predictively in perceived predation risk across landscapes. To test this hypothesis, we quantified among-individual differences in boldness and activity and exposed behaviourally phenotyped male bank voles Myodes glareolus individually to two different experimental landscapes of risks in large outdoor enclosures and provided resources as discrete food patches. We manipulated perceived predation risk via vegetation height between 2 and > 30 cm and quantified patch use indirectly via RFID-logging and giving-up densities. We statistically disentangled among-individual differences in microhabitat use from spatially varying perceived risk, i.e. landscape of fear. We found that individuals varied in mean vegetation height of their foraging microhabitats and that this microhabitat selection matched the intrinsic individual differences in perceived risk. As predicted by the patch use model, all individual's perceived higher risks when foraging in lower vegetation. However, individuals differed in their reaction norm slopes of perceived risk to vegetation height, and these differences in slopes were consistent across two different landscapes of risks and resources. We interpret these results as evidence for individual landscapes of fear, which could be predicted by among-individual differences in activity and boldness. Since perceived predation risk affects when and where to forage, among-individual differences in fear responses could act as a mode of intraspecific niche complementarity (i.e. individual niche specialization), help explain behavioural type by environment correlations, and will likely have cascading indirect effects on lower trophic levels.
The fast and the flexible
(2018)
Pregnancy termination after encountering a strange male, the Bruce effect, is regarded as a counterstrategy of female mammals towards anticipated infanticide. While confirmed in caged rodent pairs, no verification for the Bruce effect existed from experimental field populations of small rodents. We suggest that the effect may be adaptive for breeding rodent females only under specific conditions related to populations with cyclically fluctuating densities. We investigated the occurrence of delay in birth date after experimental turnover of the breeding male under different population composition in bank voles (Myodes glareolus) in large outdoor enclosures: one-male-multiple-females (n = 6 populations/18 females), multiple-males-multiplefemales (n = 15/45), and single-male-single-female (MF treatment, n = 74/74). Most delays were observed in the MF treatment after turnover. Parallel we showed in a laboratory experiment (n = 205 females) that overwintered and primiparous females, the most abundant cohort during population lows in the increase phase of cyclic rodent populations, were more likely to delay births after turnover of the male than year-born and multiparous females. Taken together, our results suggest that the Bruce effect may be an adaptive breeding strategy for rodent females in cyclic populations specifically at low densities in the increase phase, when isolated, overwintered animals associate in MF pairs. During population lows infanticide risk and inbreeding risk may then be higher than during population highs, while also the fitness value of a litter in an increasing population is higher. Therefore, the Bruce effect may be adaptive for females during annual population lows in the increase phases, even at the costs of delaying reproduction.
The Bruce effect revisited
(2017)
Pregnancy termination after encountering a strange male, the Bruce effect, is regarded as a counterstrategy of female mammals towards anticipated infanticide. While confirmed in caged rodent pairs, no verification for the Bruce effect existed from experimental field populations of small rodents. We suggest that the effect may be adaptive for breeding rodent females only under specific conditions related to populations with cyclically fluctuating densities. We investigated the occurrence of delay in birth date after experimental turnover of the breeding male under different population composition in bank voles (Myodes glareolus) in large outdoor enclosures: one-male–multiple-females (n = 6 populations/18 females), multiple-males–multiple-females (n = 15/45), and single-male–single-female (MF treatment, n = 74/74). Most delays were observed in the MF treatment after turnover. Parallel we showed in a laboratory experiment (n = 205 females) that overwintered and primiparous females, the most abundant cohort during population lows in the increase phase of cyclic rodent populations, were more likely to delay births after turnover of the male than year-born and multiparous females. Taken together, our results suggest that the Bruce effect may be an adaptive breeding strategy for rodent females in cyclic populations specifically at low densities in the increase phase, when isolated, overwintered animals associate in MF pairs. During population lows infanticide risk and inbreeding risk may then be higher than during population highs, while also the fitness value of a litter in an increasing population is higher. Therefore, the Bruce effect may be adaptive for females during annual population lows in the increase phases, even at the costs of delaying reproduction.
A fundamental focus of current ecological and evolutionary research is to illuminate the drivers of animals' success in coping with human-induced rapid environmental change (HIREC). Behavioural adaptations are likely to play a major role in coping with HIREC because behaviour largely determines how individuals interact with their surroundings. A substantial body of research reports behavioural modifications in urban dwellers compared to rural conspecifics. However, it is often unknown whether the observed phenotypic divergence is due to phenotypic plasticity or the product of genetic adaptations. Here, we aimed at investigating (a) whether behavioural differences arise also between rural and urban populations of non-commensal rodents; and (b) whether these differences result from behavioural flexibility or from intrinsic behavioural characteristics, such as genetic or maternal effects. We captured and kept under common environment conditions 42 rural and 52 urban adult common voles (Microtus arvalis) from seven subpopulations along a rural-urban gradient. We investigated individual variation in behavioural responses associated with risk-taking and exploration, in situ at the time of capture in the field and ex situ after 3 months in captivity. Urban dwellers were bolder and more explorative than rural conspecifics at the time of capture in their respective sites (in situ). However, when tested under common environmental conditions ex situ, rural individuals showed little change in their behavioural responses whereas urban individuals altered their behaviour considerably and were consistently shyer and less explorative than when tested in situ. The combination of elevated risk-taking and exploration with high behavioural flexibility might allow urban populations to successfully cope with the challenges of HIREC. Investigating whether the observed differences in behavioural flexibility are adaptive and how they are shaped by additive and interactive effects of genetic make-up and past environmental conditions will help illuminate eco-evolutionary dynamics under HIREC and predict persistence of populations under urban conditions.
Classic theories of ageing consider extrinsic mortality (EM) a major factor in shaping longevity and ageing, yet most studies of functional ageing focus on species with low EM. This bias may cause overestimation of the influence of senescent declines in performance over condition-dependent mortality on demographic processes across taxa. To simultaneously investigate the roles of functional senescence (FS) and intrinsic, extrinsic and condition-dependent mortality in a species with a high predation risk in nature, we compared age trajectories of body mass (BM) in wild and captive grey mouse lemurs (Microcebus murinus) using longitudinal data (853 individuals followed through adulthood). We found evidence of non-random mortality in both settings. In captivity, the oldest animals showed senescence in their ability to regain lost BM, whereas no evidence of FS was found in the wild. Overall, captive animals lived longer, but a reversed sex bias in lifespan was observed between wild and captive populations. We suggest that even moderately condition-dependent EM may lead to negligible FS in the wild. While high EM may act to reduce the average lifespan, this evolutionary process may be counteracted by the increased fitness of the long-lived, high-quality individuals.