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      Thermal conditions during early life influence seasonal maternal strategies in the three-spined stickleback

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          Abstract

          Background

          Conditions experienced by a female during early life may affect her reproductive strategies and maternal investment later in life. This effect of early environmental conditions is a potentially important mechanism by which animals can compensate for the negative impacts of climate change. In this study, we experimentally tested whether three-spined sticklebacks ( Gasterosteus aculeatus) change their maternal strategy according to environmental temperatures experienced earlier in life. We studied maternal investment from a life-history perspective because females are expected to adjust their reproductive strategy in relation to their current and future reproductive returns as well as offspring fitness.

          Results

          F1 families were reared in control and elevated winter temperatures and their reproductive trajectories were studied when returned to common conditions. Females that had experienced the warm winter treatment (n = 141) had a lower fecundity and reduced breeding and total lifespan compared to the control individuals (n = 159). Whereas the control females tended to produce their heaviest and largest clutches in their first reproductive attempt, the warm-acclimated females invested less in their first clutch, but then produced increasingly heavy clutches over the course of the breeding season. Egg mass increased with clutch number at a similar rate in the two groups. The warm-acclimated females increased the investment of carotenoids in the first and last clutches of the season. Thus, any transgenerational effects of the maternal thermal environment on offspring phenotype may be mediated by the allocation of antioxidants into eggs but not by egg size.

          Conclusions

          Our results indicate that conditions experienced by females during juvenile life have a profound effect on life-time maternal reproductive strategies. The temperature-induced changes in maternal strategy may be due to constraints imposed by the higher energetic costs of a warm environment, but it is possible that they allow the offspring to compensate for higher energetic costs and damage when they face the same thermal stress as did their mothers.

          Electronic supplementary material

          The online version of this article (10.1186/s12898-017-0144-x) contains supplementary material, which is available to authorized users.

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          Most cited references54

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          The adaptive significance of maternal effects

          T Mousseau (1998)
          Recently, the adaptive significance of maternal effects has been increasingly recognized. No longer are maternal effects relegated as simple `troublesome sources of environmental resemblance' that confound our ability to estimate accurately the genetic basis of traits of interest. Rather, it has become evident that many maternal effects have been shaped by the action of natural selection to act as a mechanism for adaptive phenotypic response to environmental heterogeneity. Consequently, maternal experience is translated into variation in offspring fitness.
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            Global warming benefits the small in aquatic ecosystems.

            Understanding the ecological impacts of climate change is a crucial challenge of the twenty-first century. There is a clear lack of general rules regarding the impacts of global warming on biota. Here, we present a metaanalysis of the effect of climate change on body size of ectothermic aquatic organisms (bacteria, phyto- and zooplankton, and fish) from the community to the individual level. Using long-term surveys, experimental data and published results, we show a significant increase in the proportion of small-sized species and young age classes and a decrease in size-at-age. These results are in accordance with the ecological rules dealing with the temperature-size relationships (i.e., Bergmann's rule, James' rule and Temperature-Size Rule). Our study provides evidence that reduced body size is the third universal ecological response to global warming in aquatic systems besides the shift of species ranges toward higher altitudes and latitudes and the seasonal shifts in life cycle events.
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              Maternal hormones as a tool to adjust offspring phenotype in avian species.

              Avian eggs contain substantial amounts of maternal hormones and so provide an excellent model to study hormone-mediated maternal effects. We review this new and rapidly evolving field, taking an ecological and evolutionary approach and focusing on effects and function of maternal androgens in offspring development. Manipulation of yolk levels of androgens within the physiological range indicates that maternal androgens affect behaviour, growth, morphology, immune function and survival of the offspring, in some cases even long after fledging. Descriptive and experimental studies show systematic variation in maternal androgen deposition both within and among clutches, as well as in relation to the sex of the embryo. We discuss the potential adaptive value of maternal androgen transfer at all these three levels. We conclude that maternal androgen deposition in avian eggs provides a flexible mechanism of non-genetic inheritance, by which the mother can favour some offspring over others, and adjust their developmental trajectories to prevailing environmental conditions, producing different phenotypes. However, the literature is less consistent than often assumed and at all three levels, the functional explanations need further experimental testing. The field would greatly benefit from an analysis of the underlying physiological mechanisms.
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                Author and article information

                Contributors
                yeonkim@uvigo.es
                Neil.Metcalfe@glasgow.ac.uk
                albertodss@uvigo.es
                avelando@uvigo.es
                Journal
                BMC Ecol
                BMC Ecol
                BMC Ecology
                BioMed Central (London )
                1472-6785
                10 November 2017
                10 November 2017
                2017
                : 17
                : 34
                Affiliations
                [1 ]ISNI 0000 0001 2097 6738, GRID grid.6312.6, Departamento de Ecoloxía e Bioloxía Animal, , Universidade de Vigo, ; 36310 Vigo, Spain
                [2 ]ISNI 0000 0001 2193 314X, GRID grid.8756.c, Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary and Life Sciences, , University of Glasgow, ; Glasgow, G12 8QQ UK
                Author information
                http://orcid.org/0000-0002-5170-8477
                Article
                144
                10.1186/s12898-017-0144-x
                5681783
                29126411
                3abd1da7-80cc-4274-99dd-723476efb648
                © The Author(s) 2017

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 15 June 2017
                : 2 November 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100003329, Ministerio de Economía y Competitividad;
                Award ID: CGL2014-60291-JIN
                Award ID: CGL2015-69338-C2-1-P
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000781, European Research Council;
                Award ID: 322784
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2017

                Ecology
                carotenoid,climate change,life-history,maternal effect,phenotypic plasticity
                Ecology
                carotenoid, climate change, life-history, maternal effect, phenotypic plasticity

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