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      Implications of being born late in the active season for growth, fattening, torpor use, winter survival and fecundity

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          Abstract

          For hibernators, being born late in the active season may have important effects on growth and fattening, hence on winter survival and reproduction. This study investigated differences in growth, fattening, energetic responses, winter survival and fecundity between early-born (‘EB’) and late-born (‘LB’) juvenile garden dormice ( Eliomys quercinus). LB juveniles grew and gained mass twice as fast as EB individuals. Torpor use was low during intensive growth, that are, first weeks of body mass gain, but increased during pre-hibernation fattening. LB juveniles showed higher torpor use, reached similar body sizes but lower fat content than EB individuals before hibernation. Finally, LB individuals showed similar patterns of hibernation, but higher proportion of breeders during the following year than EB dormice. These results suggest that torpor is incompatible with growth but promotes fattening and consolidates pre-hibernation fat depots. In garden dormice, being born late in the reproductive season is associated with a fast life history.

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          Garden dormice are small rodents which are common in European woodlands. They were historically widespread from Portugal in the west to the Urals (Russia) in the east. However they are now largely confined to western Europe with north-eastern and eastern populations having become scattered and fragmented. During the course of a year in northern and central Europe, they make the most of the warm season to fatten up and to produce up to two litters of youngsters. When winter comes, dormice enter hibernation, sometimes for more than six months. During this time, they must rely on their fat reserves to survive. Every year, the young from the second litter have less time to prepare for the winter compared to their siblings born earlier in the season. So, how do they still manage to get ready on time for hibernation?

          Here, Mahlert et al. studied captive pups from first and second litters for their first year, following them as they grew up, entered and then emerged from their first hibernation. The late-born individuals developed nearly twice as fast as the ones born early in the season. In fact, both reached a similar body size, but the second-litter dormice had less fat reserves. Just before their first winter, both early- and late-born animals increasingly started to enter torpor – short and daily resting-like periods when the body slows down. Torpor rarely happens when animals are growing (because growth requires a warm body), but it is useful to help storing and consolidating fat before the cold months. Late-born dormice experienced more torpor on average than their first-litter peers.

          Both groups survived their first hibernation; but when they emerged, late-born individuals were more likely to reproduce that year. In other words, the dormice which grew quickly might also have sexually matured earlier. This could suggest that animals born later in the season have a faster life history: they grow rapidly, reproduce quickly but may die younger than their early-born peers.

          Mahlert et al. highlighted how early-life events can shape the course of animals’ existences and influence how their bodies operate. It remains to be examined how these circumstances may affect the individuals in the longer term, and perhaps even their descendants.

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          Most cited references74

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          The evolution of growth trajectories: what limits growth rate?

          According to life-history theory, growth rates are subject to strong directional selection due to reproductive and survival advantages associated with large adult body size. Yet, growth is commonly observed to occur at rates lower than the maximum that is physiologically possible and intrinsic growth rates often vary among populations. This implies that slower growth is favoured under certain conditions. Realized growth rate is thus the result of a compromise between the costs and advantages of growing rapidly, and the optimal rate of growth is not equivalent to the fundamental maximum rate. The ecological and evolutionary factors influencing growth rate are reviewed, with particular emphasis on how growth might be constrained by direct fitness costs. Costs of accelerating growth might contribute to the variance in fitness that is not attributable to age or size at maturity, as well as to the variation in life-history strategies observed within and among species. Two main approaches have been taken to study the fitness trade-offs relating to growth rate. First, environmental manipulations can be used to produce treatment groups with different rates of growth. Second, common garden experiments can be used to compare fitness correlates among populations with different intrinsic growth rates. Data from these studies reveal a number of potential costs for growth over both the short and long term. In order to acquire the energy needed for faster growth, animals must increase food intake. Accordingly, in many taxa, the major constraint on growth rate appears to arise from the trade-off between predation risk and foraging effort. However, growth rates are also frequently observed to be submaximal in the absence of predation, suggesting that growth trajectories also impact fitness via other channels, such as the reallocation of finite resources between growth and other traits and functions. Despite the prevalence of submaximal growth, even when predators are absent, there is surprisingly little evidence to date demonstrating predator-independent costs of growth acceleration. Evidence that does exist indicates that such costs may be most apparent under stressful conditions. Future studies should examine more closely the link between patterns of resource allocation to traits in the adult organism and lifetime fitness. Changes in body composition at maturation, for example, may determine the outcome of trade-offs between reproduction and survival or between early and late reproduction. A number of design issues for studies investigating costs of growth that are imposed over the long term are discussed, along with suggestions for alternative approaches. Despite these issues, identifying costs of growth acceleration may fill a gap in our understanding of life-history evolution: the relationships between growth rate, the environment, and fitness may contribute substantially to the diversification of life histories in nature. © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society.
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            Natural hypometabolism during hibernation and daily torpor in mammals.

            Daily torpor and hibernation are the most powerful measures of endotherms to reduce their energy expenditure. During entrance into these torpid states metabolic rate is suppressed to a fraction of euthermic metabolism, paralleled by reductions in ventilation and heart rate. Body temperature gradually decreases towards the level of ambient temperature. In deep torpor body temperature as well as metabolic rate are controlled at a hypothermic and hypometabolic level. Torpid states are terminated by an arousal where metabolic rate spontaneously returns to normal levels again and euthermic body temperature is established by a burst of heat production. In recent years some of the cellular mechanisms which contribute to hypometabolism have been disclosed. Transcription, translation, as well as protein synthesis are largely suppressed. Cell proliferation in highly proliferating epithelia like the intestine is suspended. ATP production from glucose is reduced and lipids serve as the major substrate for remaining energy requirements. All these changes are rapidly reverted to normometabolism during arousal. Hibernation and daily torpor are found in small mammals inhabiting temperate as well as tropical climates. It indicates that this behaviour is not primarily aimed for cold defense, instead points to a general role of hypometabolism, as a measure to cope with a timely limited or seasonal bottleneck of energy supply.
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              Growth versus lifespan: perspectives from evolutionary ecology.

              There are many ecological advantages to attaining a large body size as fast as possible (such as reduced risks of being caught by predators or increased reproductive success). However, studies in several taxa indicate that fast growth in itself can have negative as well as positive effects. There appears to be a link between accelerated growth and lifespan: rapid growth early in life is associated with impaired later performance and reduced longevity. In this review we assess the evidence for such within individual trade-offs between growth rate and lifespan, and the potential physiological mechanisms that might underlie them. We discuss the fitness implications of any reduction in lifespan, and point out that certain environmental circumstances may favour a 'grow fast and die young' strategy if this increases overall reproductive success. However, investigation of the intra-specific relationships among growth rate, lifespan and fitness is not straightforward; few studies have controlled for confounding variables such as adult body size or duration of the growth period, and none to date have measured fitness in an appropriate ecological setting. We suggest a number of experimental approaches that might allow the true relationships between growth rate and future performance to be elucidated.
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                Author and article information

                Contributors
                Role: Reviewing Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                20 February 2018
                2018
                : 7
                : e31225
                Affiliations
                [1 ]deptDepartment of Integrative Biology and Evolution Research Institute of Wildlife Ecology, University of Veterinary Medicine ViennaAustria
                [2 ]Université de Strasbourg, IPHC StrasbourgFrance
                [3 ]CNRS, UMR7178 StrasbourgFrance
                [4]Max-Planck Institute for Evolutionary Biology Germany
                [5]Max-Planck Institute for Evolutionary Biology Germany
                Author information
                https://orcid.org/0000-0001-6598-9129
                https://orcid.org/0000-0001-6621-7462
                Article
                31225
                10.7554/eLife.31225
                5819945
                29458712
                62530829-57df-495e-932b-8b47a73e582e
                © 2018, Mahlert et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 13 August 2017
                : 10 January 2018
                Funding
                Funded by: University of Veterinary Medicine Vienna;
                Award ID: Postdoctoral Fellowship
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100002428, Austrian Science Fund;
                Award ID: P27267-B25
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Ecology
                Custom metadata
                Being born late in the active season is associated with a fast life history in a hibernating species, the garden dormouse ( Eliomys quercinus).

                Life sciences
                garden dormice,juveniles,hibernation,doubly-labelled water,fat reserves,life history,other
                Life sciences
                garden dormice, juveniles, hibernation, doubly-labelled water, fat reserves, life history, other

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