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      Biogeographic parallels in thermal tolerance and gene expression variation under temperature stress in a widespread bumble bee

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          Abstract

          Global temperature changes have emphasized the need to understand how species adapt to thermal stress across their ranges. Genetic mechanisms may contribute to variation in thermal tolerance, providing evidence for how organisms adapt to local environments. We determine physiological thermal limits and characterize genome-wide transcriptional changes at these limits in bumble bees using laboratory-reared Bombus vosnesenskii workers. We analyze bees reared from latitudinal (35.7–45.7°N) and altitudinal (7–2154 m) extremes of the species’ range to correlate thermal tolerance and gene expression among populations from different climates. We find that critical thermal minima (CT MIN) exhibit strong associations with local minimums at the location of queen origin, while critical thermal maximum (CT MAX) was invariant among populations. Concordant patterns are apparent in gene expression data, with regional differentiation following cold exposure, and expression shifts invariant among populations under high temperatures. Furthermore, we identify several modules of co-expressed genes that tightly correlate with critical thermal limits and temperature at the region of origin. Our results reveal that local adaptation in thermal limits and gene expression may facilitate cold tolerance across a species range, whereas high temperature responses are likely constrained, both of which may have implications for climate change responses of bumble bees.

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          Most cited references 76

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          Thermal tolerance and the global redistribution of animals

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            Ecological genomics of local adaptation.

            It is increasingly important to improve our understanding of the genetic basis of local adaptation because of its relevance to climate change, crop and animal production, and conservation of genetic resources. Phenotypic patterns that are generated by spatially varying selection have long been observed, and both genetic mapping and field experiments provided initial insights into the genetic architecture of adaptive traits. Genomic tools are now allowing genome-wide studies, and recent theoretical advances can help to design research strategies that combine genomics and field experiments to examine the genetics of local adaptation. These advances are also allowing research in non-model species, the adaptation patterns of which may differ from those of traditional model species.
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              Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation.

              Physiological thermal-tolerance limits of terrestrial ectotherms often exceed local air temperatures, implying a high degree of thermal safety (an excess of warm or cold thermal tolerance). However, air temperatures can be very different from the equilibrium body temperature of an individual ectotherm. Here, we compile thermal-tolerance limits of ectotherms across a wide range of latitudes and elevations and compare these thermal limits both to air and to operative body temperatures (theoretically equilibrated body temperatures) of small ectothermic animals during the warmest and coldest times of the year. We show that extreme operative body temperatures in exposed habitats match or exceed the physiological thermal limits of most ectotherms. Therefore, contrary to previous findings using air temperatures, most ectotherms do not have a physiological thermal-safety margin. They must therefore rely on behavior to avoid overheating during the warmest times, especially in the lowland tropics. Likewise, species living at temperate latitudes and in alpine habitats must retreat to avoid lethal cold exposure. Behavioral plasticity of habitat use and the energetic consequences of thermal retreats are therefore critical aspects of species' vulnerability to climate warming and extreme events.
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                Author and article information

                Contributors
                mlpimsler@gmail.com
                jlozier@ua.edu
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                13 October 2020
                13 October 2020
                2020
                : 10
                Affiliations
                [1 ]GRID grid.411015.0, ISNI 0000 0001 0727 7545, Department of Biological Sciences, , The University of Alabama, ; Tuscaloosa, AL 35487 USA
                [2 ]GRID grid.135963.b, ISNI 0000 0001 2109 0381, Department of Zoology and Physiology and Program in Ecology, , University of Wyoming, ; Laramie, WY 82071 USA
                [3 ]GRID grid.24827.3b, ISNI 0000 0001 2179 9593, Department of Biological Sciences, , University of Cincinnati, ; Cincinnati, OH 45221 USA
                [4 ]GRID grid.53857.3c, ISNI 0000 0001 2185 8768, USDA-ARS Pollinating Insects Research Unit, , Utah State University, ; Logan, UT 84322 USA
                [5 ]GRID grid.261331.4, ISNI 0000 0001 2285 7943, Department of Entomology, , The Ohio State University, ; Columbus, OH 44691 USA
                Article
                73391
                10.1038/s41598-020-73391-8
                7553916
                © The Author(s) 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: DEB-1457645/1457659
                Funded by: FundRef http://dx.doi.org/10.13039/100000199, US Department of Agriculture;
                Award ID: 2018-67012-28040
                Award Recipient :
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                © The Author(s) 2020

                Uncategorized

                genetic variation, evolution, physiology

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