Sex differences in telomeres and lifespan in Soay sheep: From the beginning to the end

Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/137314/1/mec14129_am.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/137314/2/mec14129.pd

How to Study Socially Monogamous Behavior in Secretive Animals? Using Social Network Analyses and Automated Tracking Systems to Study the Social Behavior of Prairie Voles

Accurately recording the social and mating behavior of wild animals is necessary to test hypotheses regarding the evolution of monogamous behavior but documenting the behavior of most wild animals is challenging. Social network analyses can use patterns of spatial and temporal co-occurrence to describe the social associations of individuals within a population, such as which opposite-sex individuals are found together more frequently than others as an indicator of their degree of social monogamy. Social networks generated using automated radio frequency identification (RFID) tracking systems may provide insights into the social behavior of secretive animals because they enable the automated and continuous tracking of the social associations among individuals, which can address many of the limitations with studying these kinds of species. We assessed the potential for social networks generated using an automated RFID tracking system to describe the social behavior of prairie voles (Microtus ochrogaster) in semi-natural enclosures. Our aim was to assess whether social networks generated using the RFID system provided meaningful insights into the social behavior of voles by comparing this method to other methods that have been traditionally used in laboratory (partner preference tests) or field (degree of home range overlap) studies to study social monogamy in prairie voles. In partner preference tests conducted in the field, females spent more time with males with which they had stronger social network associations. Voles that had stronger social network associations also had home ranges that overlapped considerably more than dyads with lower social network associations. In addition, social networks generated from live-trapping and RFID data were comparable but social networks generated using data from our RFID system recorded almost twice as many social associations overall. Our results show that social association metrics derived from social networks generated using the RFID tracking system reflect other commonly used measures of social monogamy in prairie voles. Overall, this suggests that patterns of spatial and temporal co-occurrence are meaningful measures of social monogamy in wild animals

Error management theory and the adaptive significance of transgenerational maternal‐stress effects on offspring phenotype

It is well established that circulating maternal stress hormones (glucocorticoids, GCs) can alter offspring phenotype. There is also a growing body of empirical work, within ecology and evolution, indicating that maternal GCs link the environment experienced by the mother during gestation with changes in offspring phenotype. These changes are considered to be adaptive if the maternal environment matches the offspring’s environment and maladaptive if it does not. While these ideas are conceptually sound, we lack a testable framework that can be used to investigate the fitness costs and benefits of altered offspring phenotypes across relevant future environments. We present error management theory as the foundation for a framework that can be used to assess the adaptive potential of maternal stress hormones on offspring phenotype across relevant postnatal scenarios. To encourage rigorous testing of our framework, we provide field‐testable hypotheses regarding the potential adaptive role of maternal stress across a diverse array of taxa and life histories, as well as suggestions regarding how our framework might provide insight into past, present, and future research. This perspective provides an informed lens through which to design and interpret experiments on the effects of maternal stress, provides a framework for predicting and testing variation in maternal stress across and within taxa, and also highlights how rapid environmental change that induces maternal stress may lead to evolutionary traps.This article provides a quantitative framework as a means of generating field‐testable hypotheses regarding the adaptive potential of maternal stress under different scenario combinations. By providing a mechanistic basis for examining the adaptive potential of maternal stress effects, our overall aim is not only to provide a means for explaining patterns and testing new hypotheses, but to catalyze the study of maternal stress effects under this framework across a diversity of species, life histories, and environments.Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/145404/1/ece34074_am.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/145404/2/ece34074.pd

Error management theory and the adaptive significance of transgenerational maternal-stress effects on offspring phenotype

It is well established that circulating maternal stress hormones (glucocorticoids, GCs) can alter offspring phenotype. There is also a growing body of empirical work, within ecology and evolution, indicating that maternal GCs link the environment experienced by the mother during gestation with changes in offspring phenotype. These changes are considered to be adaptive if the maternal environment matches the offspring\u27s environment and maladaptive if it does not. While these ideas are conceptually sound, we lack a testable framework that can be used to investigate the fitness costs and benefits of altered offspring phenotypes across relevant future environments. We present error management theory as the foundation for a framework that can be used to assess the adaptive potential of maternal stress hormones on offspring phenotype across relevant postnatal scenarios. To encourage rigorous testing of our framework, we provide field-testable hypotheses regarding the potential adaptive role of maternal stress across a diverse array of taxa and life histories, as well as suggestions regarding how our framework might provide insight into past, present, and future research. This perspective provides an informed lens through which to design and interpret experiments on the effects of maternal stress, provides a framework for predicting and testing variation in maternal stress across and within taxa, and also highlights how rapid environmental change that induces maternal stress may lead to evolutionary traps

Error management theory and the adaptive significance of transgenerational maternal-stress effects on offspring phenotype

It is well established that circulating maternal stress hormones (glucocorticoids, GCs) can alter offspring phenotype. There is also a growing body of empirical work, within ecology and evolution, indicating that maternal GCs link the environment experienced by the mother during gestation with changes in offspring phenotype. These changes are considered to be adaptive if the maternal environment matches the offspring\u27s environment and maladaptive if it does not. While these ideas are conceptually sound, we lack a testable framework that can be used to investigate the fitness costs and benefits of altered offspring phenotypes across relevant future environments. We present error management theory as the foundation for a framework that can be used to assess the adaptive potential of maternal stress hormones on offspring phenotype across relevant postnatal scenarios. To encourage rigorous testing of our framework, we provide field-testable hypotheses regarding the potential adaptive role of maternal stress across a diverse array of taxa and life histories, as well as suggestions regarding how our framework might provide insight into past, present, and future research. This perspective provides an informed lens through which to design and interpret experiments on the effects of maternal stress, provides a framework for predicting and testing variation in maternal stress across and within taxa, and also highlights how rapid environmental change that induces maternal stress may lead to evolutionary traps

Equipped for Life in the Boreal Forest: The Role of the Stress Axis in Mammals

The hypothalamic-pituitary-adrenal axis (stress axis) plays a central role in equipping mammals to succeed in the challenging environment of the boreal forest. Over the last 20 years, we have tackled a broad range of topics to understand how the stress axis functions in four key herbivore species. The central challenge for snowshoe hares is coping with their predators, whereas for the others, it is primarily coping with each other (especially during reproduction) and with their physical environment. Hares are severely stressed by their predators during the population decline. The predator threat causes major changes in the stress axis of hares and reduces their reproduction; in addition, acting through maternal programming, it is the most plausible explanation for the extended period of low numbers following the population decline. Arctic ground squirrel males have an intense breeding season for two to three weeks in early spring, after which many of them die. The functioning of their stress axis changes markedly and is key in meeting their energy demands during this period. In contrast, red-backed vole males, though also short-lived, breed repeatedly only in the summer of their life, and their stress axis shows no change in function. However, their reproductive effort negatively affects their long-term survival. Territorial red squirrels experience marked interannual fluctuations in their major food source (white spruce seed), resulting in major fluctuations in their densities and consequently in the intensity of territorial competition. Changes in the densities of red squirrels also alter maternal stress hormone levels, inducing adaptive plasticity in offspring postnatal growth rates that prepares offspring for the environment they will encounter at independence. To survive winter, red squirrels need to defend their territories year-round, and the basis of this defense appears to be adrenal dehydroepiandrosterone, which has the benefits, but not the costs, of gonadal steroids. Arctic ground squirrels survive winter by hibernating in deeply frozen ground. Unlike all other hibernators, they have evolved a unique adaptation: high levels of adrenal androgens in summer to accumulate protein reserves that they then burn in winter. With a rapidly changing climate, the stress axis will play a key role in permitting northern animals to adapt, but the linkages between the changes in the abiotic and biotic components of the boreal forest and the phenotypic plasticity in the stress response of its inhabitants are not well understood for these or any other herbivore species.L’axe hypothalamo-hypophyso-surrénalien (l’axe du stress) joue un rôle central pour aider les mammifères à réussir dans l’environnement difficile de la forêt boréale. Ces 20 dernières années, nous nous sommes penchés sur une vaste gamme de sujets afin de comprendre comment fonctionne l’axe du stress chez quatre grandes espèces herbivores. Pour le lièvre d’Amérique, le défi central consiste à faire face à ses prédateurs, tandis que pour les autres espèces, ce défi consiste à se faire face mutuellement (surtout pendant la reproduction) de même qu’à faire face à leur environnement physique. Les lièvres subissent beaucoup de stress de la part de leurs prédateurs pendant la diminution de la population. La menace des prédateurs est la cause de changements majeurs sur l’axe du stress des lièvres, ce qui a pour effet de réduire leur reproduction. De plus, en raison de leur programmation maternelle, il s’agit de l’explication la plus plausible justifiant la période prolongée de leur faible nombre suivant la diminution de la population. Le spermophile arctique mâle a une période de reproduction intense pendant deux à trois semaines au début du printemps et après cela, un grand nombre d’entre eux meurent. Le fonctionnement de son axe de stress change de façon marquée, ce qui est essentiel à sa demande en énergie pendant cette période. Par contraste, le campagnol à dos roux mâle, même s’il ne vit également pas longtemps, se reproduit à répétition seulement pendant l’été de sa vie, et le fonctionnement de son axe de stress ne montre aucun changement. Cependant, ses efforts de reproduction ont des incidences négatives sur sa survie à long terme. Pour sa part, la principale source d’alimentation (les graines d’épinette blanche) de l’écureuil roux territorial connaît des fluctuations interannuelles marquées, ce qui se traduit par une fluctuation majeure en matière de densité de cette espèce animale et, par conséquent, en matière d’intensité de la concurrence pour le territoire. Les changements de densité d’écureuils roux exercent également une influence sur les taux d’hormone maternelle de stress, ce qui donne lieu à une plasticité adaptative des taux de croissance postnatale de la progéniture qui prépare la progéniture pour faire face à l’environnement dans lequel ils évolueront au stade de l’indépendance. Pour survivre à l’hiver, l’écureuil roux doit défendre son territoire à l’année et pour y parvenir, il se sert de la déhydroépiandrostérone surrénalienne, qui comporte les avantages des stéroïdes gonades, sans les coûts. Le spermophile arctique survit à l’hiver en hibernant dans le sol gelé en profondeur. Contrairement à tous les autres hibernateurs, il s’est développé une adaptation unique en son genre, soit des taux élevés d’androgènes surrénaliens en été qui lui permettent d’accumuler les réserves de protéines qu’il brûle ensuite pendant l’hiver. À la lumière du changement climatique rapide, l’axe de stress jouera un rôle-clé pour permettre aux animaux du Nord de s’adapter, mais les liens entre les changements des composantes abiotiques et biotiques de la forêt boréale et la plasticité phénotypique de la réaction de stress de ses habitants ne sont pas bien compris dans le cas de ces espèces herbivores ou de toute autre espèce herbivore

Social conflict and costs of cooperation in meerkats are reflected in measures of stress hormones

Measures of glucocorticoid stress hormones (e.g. cortisol) have often been used to characterize conflict between subordinates and dominants. In cooperative breeders where subordinates seldom breed in their natal group and assist in offspring rearing, increases in subordinate glucocorticoid levels may be caused by conflict among subordinates as well as by the energetic costs of helping behavior and fluctuations in food availability may exacerbate these effects. During a 6-year study of Kalahari meerkats (Suricata suricatta), we investigated how social, environmental, and individual characteristics influenced subordinate plasma cortisol levels. Subordinate females, who are often the target of aggression from dominant females, had higher cortisol levels when the dominant female in their group was pregnant while the cortisol levels of subordinate males were unaffected by the reproductive state of dominant females. Subordinates of both sexes had higher cortisol levels if they belonged to groups 1) where neither of the dominant breeders in the group were their parents, 2) that contained a high proportion of subordinate females, or 3) that were either very large or very small, especially when the weather was cold and dry. Subordinates in groups containing young pups had higher cortisol levels. Finally, cortisol levels were higher in subordinates of both sexes if they were lighter for their age or had lost little body mass the night prior to sampling. Our results show that both social conflict and cooperative behavior can elevate glucocorticoid levels in subordinates and that both effects can be modified by variation in weather and food availability.The National Environment Research Council (RG53472 to T.H.C-B.), the European Research Council (294494 to T.H.C-B.), the University of Zurich and the Mammal Research Institute at the University of Pretoria.http://beheco.oxfordjournals.org2018-07-01hj2018Mammal Research InstituteZoology and Entomolog

Rank-related contrasts in longevity arise from extra-group excursions not delayed senescence in a cooperative mammal

In many cooperatively breeding animal societies, breeders outlive non-breeding subordinates, despite investing heavily in reproduction [1-3]. In eusocial insects, the extended lifespans of breeders arise from specialized slowed aging profiles [1], prompting suggestions that reproduction and dominance similarly defer aging in cooperatively breeding vertebrates, too [4-6]. Although lacking the permanent castes of eusocial insects, breeders of vertebrate societies could delay aging via phenotypic plasticity (similar rank-related changes occur in growth, neuroendocrinology, and behavior [7-10]), and such plastic deferment of aging may reveal novel targets for preventing aging-related diseases [11]. Here, we investigate whether breeding dominants exhibit extended longevity and delayed age-related physiological declines in wild cooperatively breeding meerkats. We show that dominants outlive subordinates but exhibit faster telomere attrition (a marker of cellular senescence and hallmark of aging [12]) and that in dominants (but not subordinates), rapid telomere attrition is associated with mortality. Our findings further suggest that, rather than resulting from specialized aging profiles, differences in longevity between dominants and subordinates are driven by subordinate dispersal forays, which become exponentially more frequent with age and increase subordinate mortality. These results highlight the need to critically examine the causes of rank-related longevity contrasts in other cooperatively breeding vertebrates, including social mole-rats, where they are currently attributed to specialized aging profiles in dominants [4]

Social conflict and costs of cooperation in meerkats are reflected in measures of stress hormones

Measures of glucocorticoid stress hormones (e.g. cortisol) have often been used to characterize conflict between subordinates and dominants. In cooperative breeders where subordinates seldom breed in their natal group and assist in offspring rearing, increases in subordinate glucocorticoid levels may be caused by conflict among subordinates as well as by the energetic costs of helping behavior and fluctuations in food availability may exacerbate these effects. During a 6-year study of Kalahari meerkats (Suricata suricatta), we investigated how social, environmental, and individual characteristics influenced subordinate plasma cortisol levels. Subordinate females, who are often the target of aggression from dominant females, had higher cortisol levels when the dominant female in their group was pregnant while the cortisol levels of subordinate males were unaffected by the reproductive state of dominant females. Subordinates of both sexes had higher cortisol levels if they belonged to groups 1) where neither of the dominant breeders in the group were their parents, 2) that contained a high proportion of subordinate females, or 3) that were either very large or very small, especially when the weather was cold and dry. Subordinates in groups containing young pups had higher cortisol levels. Finally, cortisol levels were higher in subordinates of both sexes if they were lighter for their age or had lost little body mass the night prior to sampling. Our results show that both social conflict and cooperative behavior can elevate glucocorticoid levels in subordinates and that both effects can be modified by variation in weather and food availability.The National Environment Research Council (RG53472 to T.H.C-B.), the European Research Council (294494 to T.H.C-B.), the University of Zurich and the Mammal Research Institute at the University of Pretoria.http://beheco.oxfordjournals.org2018-07-01hj2018Mammal Research InstituteZoology and Entomolog

Indirect effects on fitness between individuals that have never met via an extended phenotype

Interactions between organisms are ubiquitous and have important consequences for phenotypes and fitness. Individuals can even influence those they never meet, if they have extended phenotypes that alter the environments others experience. North American red squirrels (Tamiasciurus hudsonicus) guard food hoards, an extended phenotype that typically outlives the individual and is usually subsequently acquired by non‐relatives. Hoarding by previous owners can, therefore, influence subsequent owners. We found that red squirrels breed earlier and had higher lifetime fitness if the previous hoard owner was a male. This was driven by hoarding behaviour, as males and mid‐aged squirrels had the largest hoards, and these effects persisted across owners, such that if the previous owner was male or died in mid‐age, subsequent occupants had larger hoards. Individuals can, therefore, influence each other’s resource‐dependent traits and fitness without ever meeting, such that the past can influence contemporary population dynamics through extended phenotypes.Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/148423/1/ele13230.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/148423/2/ele13230_am.pd