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      When water interacts with temperature: Ecological and evolutionary implications of thermo‐hydroregulation in terrestrial ectotherms

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          Abstract

          The regulation of body temperature (thermoregulation) and of water balance (defined here as hydroregulation) are key processes underlying ecological and evolutionary responses to climate fluctuations in wild animal populations. In terrestrial (or semiterrestrial) ectotherms, thermoregulation and hydroregulation closely interact and combined temperature and water constraints should directly influence individual performances. Although comparative physiologists traditionally investigate jointly water and temperature regulation, the ecological and evolutionary implications of these coupled processes have so far mostly been studied independently. Here, we revisit the concept of thermo‐hydroregulation to address the functional integration of body temperature and water balance regulation in terrestrial ectotherms. We demonstrate how thermo‐hydroregulation provides a framework to investigate functional adaptations to joint environmental variation in temperature and water availability, and potential physiological and/or behavioral conflicts between thermoregulation and hydroregulation. We extend the classical cost–benefit model of thermoregulation in ectotherms to highlight the adaptive evolution of optimal thermo‐hydroregulation strategies. Critical gaps in the parameterization of this conceptual optimality model and guidelines for future empirical research are discussed. We show that studies of thermo‐hydroregulation refine our mechanistic understanding of physiological and behavioral plasticity, and of the fundamental niche of the species. This is illustrated with relevant and recent examples of space use and dispersal, resource‐based trade‐offs, and life‐history tactics in insects, amphibians, and nonavian reptiles.

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          The potential for behavioral thermoregulation to buffer "cold-blooded" animals against climate warming.

          Increasing concern about the impacts of global warming on biodiversity has stimulated extensive discussion, but methods to translate broad-scale shifts in climate into direct impacts on living animals remain simplistic. A key missing element from models of climatic change impacts on animals is the buffering influence of behavioral thermoregulation. Here, we show how behavioral and mass/energy balance models can be combined with spatial data on climate, topography, and vegetation to predict impacts of increased air temperature on thermoregulating ectotherms such as reptiles and insects (a large portion of global biodiversity). We show that for most "cold-blooded" terrestrial animals, the primary thermal challenge is not to attain high body temperatures (although this is important in temperate environments) but to stay cool (particularly in tropical and desert areas, where ectotherm biodiversity is greatest). The impact of climate warming on thermoregulating ectotherms will depend critically on how changes in vegetation cover alter the availability of shade as well as the animals' capacities to alter their seasonal timing of activity and reproduction. Warmer environments also may increase maintenance energy costs while simultaneously constraining activity time, putting pressure on mass and energy budgets. Energy- and mass-balance models provide a general method to integrate the complexity of these direct interactions between organisms and climate into spatial predictions of the impact of climate change on biodiversity. This methodology allows quantitative organism- and habitat-specific assessments of climate change impacts.
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            The evolution of thermal physiology in ectotherms

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              Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches

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                Author and article information

                Contributors
                david.rozen-rechels@normalesup.org
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                02 August 2019
                September 2019
                : 9
                : 17 ( doiID: 10.1002/ece3.v9.17 )
                : 10029-10043
                Affiliations
                [ 1 ] Sorbonne Université, UPEC, CNRS, IRD INRA Institut d'Écologie et des Sciences de l'Environnement, IEES Paris France
                [ 2 ] UMR 5321 CNRS-Université Toulouse III Paul Sabatier Station d'Écologie Théorique et Expérimentale Moulis France
                [ 3 ] UMR 7372 CNRS-ULR Centre d'Études Biologiques de Chizé Villiers en Bois France
                [ 4 ] School of Life Sciences Arizona State University Tempe AZ USA
                [ 5 ] CNRS, Univ Montpellier, EPHE, IRD, Univ Paul Valéry Montpellier 3 Centre d'Écologie Fonctionnelle et Évolutive Montpellier France
                [ 6 ] Sorbonne Université ESPE de Paris Paris France
                [ 7 ] École normale supérieure, CNRS, UMS 3194 Centre de recherche en écologie expérimentale et prédictive (CEREEP‐Ecotron IleDeFrance), Département de biologie PSL Research University Saint‐Pierre‐lès‐Nemours France
                Author notes
                [*] [* ] Correspondence

                David Rozen‐Rechels, Sorbonne Université, UPEC, CNRS, IRD, INRA, Institut d'Écologie et des Sciences de l'Environnement, IEES, Paris, France.

                Email: david.rozen-rechels@ 123456normalesup.org

                Author information
                https://orcid.org/0000-0003-4351-8961
                https://orcid.org/0000-0002-2501-464X
                Article
                ECE35440
                10.1002/ece3.5440
                6745666
                31534711
                8e785b67-bede-4888-bff0-7538e99ff849
                © 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 15 May 2019
                : 17 June 2019
                Page count
                Figures: 3, Tables: 1, Pages: 15, Words: 12363
                Funding
                Funded by: Agence Nationale de la Recherche
                Award ID: ANR-16-CE02-0001
                Award ID: ANR-17-CE02-0013
                Funded by: Région Nouvelle Aquitaine
                Funded by: Ministère de l'Enseignement Supérieur et de la Recherche
                Categories
                Hypotheses
                Hypotheses
                Custom metadata
                2.0
                ece35440
                September 2019
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.6.9 mode:remove_FC converted:16.09.2019

                Evolutionary Biology
                behavioral decisions,body temperature,performance curves,physiological adjustments,water balance

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