Patrick Bergeron

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.

Individual quality: tautology or biological reality?

Heterogeneity among individuals is a central aspect of evolutionary ecology. Evolutionary changes of a population depend on selection pressures acting on individual’s phenotypic and genetic variation (Lynch & Walsh 1998). Individuals are rarely equally adapted to their environments, and this inter-individual heterogeneity in performance (e.g. survival and reproductive success) has been historically described with a variety of terms such as heterogeneity in fit (Darwin 1859), frailty (Vaupel, Manton & Stallard 1979), health and vigour (Hamilton & Zuk 1982) or organism’s state (McNamara & Houston 1996). Nowadays, a growing number of studies in animal behaviour, population biology and evolutionary ecology refer to inter-individual variations as differences in ‘quality’ (e.g. Birds: Sedinger et al. 2008; Mammals: Hamel et al. 2009; Insects: Cervo et al. 2008; Fishes: Wong, Candolin & Lindstrom 2007). However, since many studies have sought to measure ‘individual quality’ itself, there are many definitions of this concept. Recently, Wilson & Nussey (2010) proposed the following working definition of quality: ‘an axis of among-individual heterogeneity that is positively correlated with fitness’. This definition summarizes well the general acceptance that quality indices mostly relate an individual’s characteristics (phenotype or genotype) to fitness parameters. Yet, the choice of a quality index is always dictated by the study focus or species rather than by a general acceptance of what traits best describe quality. In fact, using different types of quality traits from a variety of conceptual frameworks may prevent researchers from adopting a single definition of quality. Here, we highlight four key distinctions between the views and uses of quality. We emphasize that relabelling other well-established terms (i.e. fitness) under the concept of quality may only bring further confusion. Instead, we suggest three recommendations to help authors being more explicit about their applications of this concept and to facilitate the comparison among studies using similar conceptual frameworks.

Anticipation and tracking of pulsed resources drive population dynamics in eastern chipmunks

Pulsed systems are characterized by boom and bust cycles of resource production that are expected to cascade through multiple trophic levels. Many of the consumers within pulsed resource systems have specific adaptations to cope with these cycles that may serve to either amplify or dampen their community-wide consequences. We monitored a seed predator, the eastern chipmunk (Tamias striatus), in an American beech (Fagus grandifolia) dominated forest, and used capture-mark-recapture analyses to estimate chipmunk vital rates and relate them to interannual variation in beech seed production. The summer activity and reproduction of adults anticipated autumn beech production, with high activity and intense reproduction occurring in summers prior to beech masts. Chipmunks also reproduced every spring following a beech mast. However, adult survival was independent of beech production. In contrast, juvenile survival was lower in years of mast failure than in years of mast production, but their activity was consistently high and independent of beech production. Population growth was strongly affected by the number of juveniles and therefore by beech seed production, which explains nearly 70% of variation in population growth. Our results suggest that a combination of resource-dependent reproduction and variable activity levels associated with anticipation and response to resource pulses allows consumers to buffer potential deleterious effects of low food abundance on their survival.

Secondary sexual characters signal fighting ability and determine social rank in Alpine ibex ( Capra ibex )

Social dominance is a fundamental aspect of male evolutionary ecology in polygynous mammals because it determines access to estrous females. As it is rarely possible to monitor marked individuals of known morphology, little is known about the determinants of male dominance. We studied the social structure of Alpine ibex males in Gran Paradiso National Park, Italy in 2003, 2006, and 2007. Dominance interactions produced a linear social hierarchy. In ibex males, body mass and horn length are key traits in male-male combat, and both increase with age. We explored the links between age, body mass, horn length, and social rank. Ibex males showed much age-independent phenotypic heterogeneity and rapidly growing males reached high rank at a younger age than slow-growing males. Because there is no trade-off between horn growth and longevity, fast-growing males may face weak potential costs of rapid growth and high fitness benefit of achieving high rank. Violent interactions were more likely to occur between males similar in both mass and horn length, independently of age. We suggest that only high-quality individuals can afford a strategy of rapid growth for both secondary sexual characters, and likely reap substantial fitness benefits.

Detection of a Novel, Integrative Aging Process Suggests Complex Physiological Integration

Many studies of aging examine biomarkers one at a time, but complex systems theory and network theory suggest that interpretations of individual markers may be context-dependent. Here, we attempted to detect underlying processes governing the levels of many biomarkers simultaneously by applying principal components analysis to 43 common clinical biomarkers measured longitudinally in 3694 humans from three longitudinal cohort studies on two continents (Women’s Health and Aging I & II, InCHIANTI, and the Baltimore Longitudinal Study on Aging). The first axis was associated with anemia, inflammation, and low levels of calcium and albumin. The axis structure was precisely reproduced in all three populations and in all demographic sub-populations (by sex, race, etc.); we call the process represented by the axis “integrated albunemia.” Integrated albunemia increases and accelerates with age in all populations, and predicts mortality and frailty – but not chronic disease – even after controlling for age. This suggests a role in the aging process, though causality is not yet clear. Integrated albunemia behaves more stably across populations than its component biomarkers, and thus appears to represent a higher-order physiological process emerging from the structure of underlying regulatory networks. If this is correct, detection of this process has substantial implications for physiological organization more generally.

Parallel Lasers for Remote Measurements of Morphological Traits

Abstract Animal ecology research could benefit from the measurement of individual morphological traits. In bovids, male horn size often correlates with annual reproductive success, is sensitive to resource abundance, and could be a predictor of survival. However, live captures are costly, involve some risk of injury or substantial disturbance to the animals, and are impossible in many situations. To remotely measure horn growth of free-ranging Alpine ibex (Capra ibex), I designed an aluminum frame that holds parallel laser pointers and a digital camera. I took digital pictures of ibex horns and calculated horn growth based on the fixed distance between the 2 laser points. This simple and accurate technique could benefit many ecological studies that require linear measurements, such as shoulder height, body length, leg length, or fin length. It could also help measure body features (e.g., fur or skin patterns, scars), increasing the reliability of individual photographic identification.

Pulsed resources and the coupling between life-history strategies and exploration patterns in eastern chipmunks (Tamias striatus)

Understanding the causes of animal personality (i.e. consistent behavioural differences) is a major aim of evolutionary studies. Recent theoretical work suggests that major personality traits may contribute to evolutionary trade-offs. However, such associations have only been investigated in a few study systems, and even less so in free ranging animal populations. Eastern chipmunks exhibit consistent individual differences in exploration, ranging from slow to fast. Birth cohorts also experience dramatic differences in age at first breeding opportunity due to annual differences in beech mast. Individuals may breed for the first time at 24, 33 or 50% of their average life span, depending on year of birth. Here, we used data from a long-term survey on a wild population to investigate the relationship between reproductive life history and consistent individual differences in exploration. We determined whether predictable differences in age at first breeding opportunity among birth cohorts were associated with exploration differences and favoured individuals with different exploration. Birth cohorts with a predictably earlier age at first breeding opportunity were faster explorers on average. Slower explorers displayed their highest fecundity (females) or highest fertilization success (males) later in their life compared with faster explorers. Overall, slow explorers attained a higher lifetime reproductive success than fast explorers when given an opportunity to reproduce later in their life. Our results suggest that the timing of mating seasons, associated with fluctuating food abundance, may favour individual variation in exploration and maintain population variation through its effects on reproductive life history. Together, our result shed light on how fluctuation in ecological conditions may maintain personality differences and on the nature of the relationships between animal personality and life history.

Evidence of multiple paternity and mate selection for inbreeding avoidance in wild eastern chipmunks

Mate selection for inbreeding avoidance is documented in several taxa. In mammals, most conclusive evidence comes from captive experiments that control for the availability of mates and for the level of genetic relatedness between mating partners. However, the importance of mate selection for inbreeding avoidance as a determinant of siring success in the wild has rarely been addressed. We followed the reproduction of a wild population of eastern chipmunks (Tamias striatus) during five breeding seasons between 2006 and 2009. Using molecular tools and parentage assignment methods, we found that multiple paternity (among polytocous litters) varied from 25% in an early‐spring breeding season when less than a quarter of females in the population were reproductively active to 100% across three summer breeding seasons and one spring breeding season when more than 85% of females were reproductively active. Genetically related parents were common in this population and produced less heterozygous offspring. Furthermore, litters with multiple sires showed a higher average relatedness among partners than litters with only a single sire. In multiply sired litters, however, males that were more closely related to their partners sired fewer offspring. Our results corroborate findings from captive experiments and suggest that selection for inbreeding avoidance can be an important determinant of reproductive success in wild mammals.

Homeostatic dysregulation proceeds in parallel in multiple physiological systems

An increasing number of aging researchers believes that multi‐system physiological dysregulation may be a key biological mechanism of aging, but evidence of this has been sparse. Here, we used biomarker data on nearly 33 000 individuals from four large datasets to test for the presence of multi‐system dysregulation. We grouped 37 biomarkers into six a priori groupings representing physiological systems (lipids, immune, oxygen transport, liver function, vitamins, and electrolytes), then calculated dysregulation scores for each system in each individual using statistical distance. Correlations among dysregulation levels across systems were generally weak but significant. Comparison of these results to dysregulation in arbitrary ‘systems’ generated by random grouping of biomarkers showed that a priori knowledge effectively distinguished the true systems in which dysregulation proceeds most independently. In other words, correlations among dysregulation levels were higher using arbitrary systems, indicating that only a priori systems identified distinct dysregulation processes. Additionally, dysregulation of most systems increased with age and significantly predicted multiple health outcomes including mortality, frailty, diabetes, heart disease, and number of chronic diseases. The six systems differed in how well their dysregulation scores predicted health outcomes and age. These findings present the first unequivocal demonstration of integrated multi‐system physiological dysregulation during aging, demonstrating that physiological dysregulation proceeds neither as a single global process nor as a completely independent process in different systems, but rather as a set of system‐specific processes likely linked through weak feedback effects. These processes – probably many more than the six measured here – are implicated in aging.

Disruptive viability selection on adult exploratory behaviour in eastern chipmunks

Heterogeneous forces of selection associated with fluctuating environments are recognized as important factors involved in the maintenance of inter‐individual phenotypic variance within populations. Consistent behavioural differences over time and across situations (e.g. personality) are increasingly cited as examples of individual variation observed within populations. However, the suggestion that heterogeneous selective pressures target different animal personalities remains largely untested in the wild. In this 5‐year study, we investigated the dynamics of viability selection on a personality trait, exploration, in a population of eastern chipmunks (Tamias striatus) experiencing substantial seasonal variations in weather conditions and food availability associated with masting trees. Contrary to our expectations, we found no evidence of fluctuating selection on exploration. Instead, we found strong disruptive viability selection on adult exploration behaviour, independent of seasonal variations. Individuals with either low or high exploration scores were almost twice as likely to survive over a 6‐month period compared with individuals with intermediate scores. We found no evidence of viability selection on juvenile exploration. Our results highlight that disruptive selection might play an important role in the maintenance of phenotypic variance of wild populations through its effect on different personality types across temporally varying environmental conditions.