EDITORIAL published: 13 January 2021 doi: 10.3389/fgene.2020.619441 Editorial: Coping With Climate Change: A Genomic Perspective on Thermal Adaptation Margarida Matos 1*, Pedro Simões 1 , Inês Fragata 1 , Ana Sofia Quina 2 , Torsten Nygaard Kristensen 3 and Mauro Santos 4 1 cE3c – Centre for Ecology, Evolution and Environmental Changes, Faculdade de Ciências, Universidade de Lisboa, Lisbon, Portugal, 2 CESAM, Centre for Environmental and Marine Studies, Universidade de Aveiro and Faculdade de Ciências, Universidade de Lisboa, Lisbon, Portugal, 3 Section of Biology and Environmental Science, Department of Chemistry and Bioscience, Aalborg University, Aalborg, Denmark, 4 Departament de Genètica i de Microbiologia, Grup de Genòmica, Bioinformàtica i Biologia Evolutiva (GBBE), Universitat Autònoma de Barcelona, Barcelona, Spain Keywords: candidate genes for thermal adaptation, genomic basis of evolutionary potential, genome-wide association studies, transcriptomics, thermal plasticity Editorial on the Research Topic Coping With Climate Change: A Genomic Perspective on Thermal Adaptation Current human-induced climate warming poses a threat to many organisms (Somero, 2012; Buckley and Huey, 2016; Walsh et al., 2019). Species respond to climate change in different ways, from plasticity, evolutionary adaptation, and dispersal, to extinction (Holt, 1990; Parmesan, 2006). In ectotherms, the upper thermal limits have limited plasticity compared to lower thermal limits (Gunderson and Stillman, 2015). Additionally, physiological tolerance to critically high temperatures (when performance drops to zero) may be genetically constrained (Araújo et al., Edited and reviewed by: 2013; Hoffmann et al., 2013). Consequently, behavioral thermoregulation can be an important Samuel A. Cushman, United States Forest Service (USDA), mechanism in buffering exposure to extreme temperatures (Sunday et al., 2014). Predicting how United States species may adapt to new thermal conditions requires robust ways of evaluating their underlying *Correspondence: evolutionary and plastic potentials. Given that intraspecific differentiation to upper critical thermal Margarida Matos limits is commonly observed (e.g., Herrando-Pérez et al., 2019, 2020), selection for tolerance to high mmmatos@fc.ul.pt temperatures may be occurring, although it is not clear how. This calls for a deeper understanding of the underlying genetic basis of thermal adaptation (Porcelli et al., 2015). Specialty section: In recent decades there has been a boom in studies that use genome-wide sequencing This article was submitted to (Savolainen et al., 2013; Ellegren, 2014). Next-generation sequencing techniques, when applied Evolutionary and Population Genetics, to experimental thermal evolution have contributed to understanding these genomic responses a section of the journal to changing thermal conditions (e.g., Porcelli et al., 2015; Mallard et al., 2018). The combination Frontiers in Genetics of genome-wide screenings with more classical approaches could pave the way for an integrative Received: 20 October 2020 understanding of how populations cope with climate change. This Research Topic aims to: (1) Accepted: 15 December 2020 expand knowledge on the genomic basis of thermal adaptation; (2) assess whether and how genetic Published: 13 January 2021 and genomic diversity can lead to common or different adaptive routes; and (3) discuss ways to Citation: improve the contribution of different studies to community-level knowledge. Matos M, Simões P, Fragata I, Logan and Cox suggest that there is moderate heritability for upper thermal tolerance and, Quina AS, Kristensen TN and Santos M (2021) Editorial: Coping hence, the potential for heat tolerance to evolve. However, this may also be constrained by With Climate Change: A Genomic unfavorable genetic correlations with other thermal performance traits. They also suggest that Perspective on Thermal Adaptation. the plastic response of the transcriptome depends on the magnitude of thermal shifts. Rodrigues Front. Genet. 11:619441. and Beldade also study genomics and transcriptomics of plasticity, which are usually assumed to doi: 10.3389/fgene.2020.619441 have the potential to enhance thermal adaptation. However, more research is needed because high Frontiers in Genetics | www.frontiersin.org 1 January 2021 | Volume 11 | Article 619441 Matos et al. Editorial: The Genomics of Thermal Adaptation phenotypic plasticity may be maladaptive in warmer and more Wolbachia infecting D. melanogaster lines evolved in cold and variable future climates (Kreyling et al., 2019). hot environments, and found that these dynamics cannot be Using a genome-wide association study and transcriptomic straightforwardly linked to temperature, making it difficult to profiling in lines from the Drosophila Genetic Reference predict the impact of climate change. Panel (DGRP, Mackay et al., 2012), Lecheta et al. found A goal of genome-wide analyses is to detect and understand that heat tolerance is less variable than cold tolerance, with the signatures left by natural selection on the genome. Cortés ∼50% more identified genes affecting the latter. These results et al. summarize some of the tools available to reveal the genetic reinforce that heat tolerance is more constrained than cold consequences of climate change, but there are some shortcomings tolerance (Araújo et al., 2013). However, all lines came from to linking fitness relevant genes with environmental factors; e.g., one single population, which could produce biased estimates those related to data reporting as highlighted by Waldvogel et al. of heat tolerance (Herrando-Pérez et al., 2020), and further This is important, as genotype-environment associations can be a research in other populations is needed. The Research Topic key ingredient in forecasting the response of natural populations also includes genome-wide approaches and gene expression to climatic variation. analyses. Sørensen et al. studied D. simulans populations after Relevant insights into the genetic basis of thermal evolution 20 generations of experimental evolution under predictable can come from studying the adaptations of organisms that live in or unpredictable thermal fluctuations. The strongest response extreme natural environments. Using a metagenomics approach, involved unpredictable fluctuations, and the genes under Alcorta et al. shed light on the genomic features and taxonomy of selection were distinct from the genes that are important for the thermophilic cyanobacteria living in hot springs. These features adaptive plastic response under predictive thermal fluctuations. included genome reduction, changes in GC content, coding Other studies have shown that constant and fluctuating density, and size of biosynthetic gene clusters. temperatures induce different plastic and evolutionary responses The contributions to this Research Topic add to our (Botero et al., 2015; Dey et al., 2016), and more studies like this are understanding of thermal adaptation and its multifactorial important in uncovering the complexities of thermal evolution. nature, and highlight the challenges that are still ahead of us in A potential limitation of studies on the evolution of heat striving for a deeper understanding of adaptation to expected tolerance is that most ignore the possible negative impacts of higher and more variable future temperatures. As shown in this sublethal temperatures on oogenesis and spermatogenesis. This Research Topic, increased knowledge should be brought about could lead to a higher vulnerability to climate warming in many by complementary approaches comprising different levels of organisms than is currently thought (David et al., 2005; Walsh biological organization and their interaction, using a variety of et al., 2019). Using the DGRP, Zwoinska et al. found that males methodologies and study organisms. are more affected than females when flies were exposed at high sublethal temperatures. At the same time, they did not find AUTHOR CONTRIBUTIONS additive genetic variance for reproductive performance at these temperatures. Similar results were obtained for the egg-to-adult All authors listed have made a substantial, direct and intellectual viability assessed at different temperatures in D. melanogaster contribution to the work, and approved it for publication. All (Kristensen et al., 2015). However, in Zwoinska et al. the power to authors contributed to the writing of the editorial. map the genetic variants of relatively small effects may be reduced due to the low line number. Thus more studies, using several FUNDING populations or more DGRP lines are needed. Few studies have demonstrated that adaptive evolution is MM and PS research received funding by Fundação para a occurring as a consequence of climate change. Latitudinal and Ciência e a Tecnologia (FCT) for the projects PTDC/BIA- long-term trends in the frequency of inversions in Drosophila EVL/28298/2017 and cE3c Unit UIDB/BIA/00329/2020. PS and subobscura are remarkably consistent worldwide and highly AQ are funded by FCT through a contract foreseen in ns. correlated with environmental temperature, respond to seasonal 4–6 of article 23 of DL 57/2016, changed by Law 57/2017. changes and frequency shifts shortly after a heatwave (Balanyà IF was funded by a Junior Researcher contract from FCT et al., 2006; Rezende et al., 2010; Rodríguez-Trelles et al., (CEECIND/02616/2018). TK was supported by grants from the 2013). Karageorgiou et al. focused on the breakpoints of a Danish Council for Independent Research (DFF-8021-00014B). particular inversion that shows cyclic seasonal changes and MS was funded by grants CGL2017-89160P from the Ministerio speculate that this might be partly due to antagonistic pleiotropic de Economía y Competitividad (Spain; co-financed with the effects on reproduction and immunity resulting from a position European Union FEDER funds), and 2017SGR 1379 from effect affecting the expression of functional genes located at Generalitat de Catalunya. the breakpoints. An important ingredient in a warming world is the ecological ACKNOWLEDGMENTS and evolutionary implications of parasite-host dynamics and prevalence. Mazzucco et al. focussed on the endosymbiont We are grateful to all contributors to this Research Topic. Frontiers in Genetics | www.frontiersin.org 2 January 2021 | Volume 11 | Article 619441 Matos et al. 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