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1. Genetic and physiological mechanisms of freezing tolerance in locally adapted populations of a winter annual

   https://doi.org/10.1002/ajb2.1385  

   Sanderson, Brian J. ; Park, Sunchung ; Jameel, M. Inam ; Kraft, Joshua C. ; Thomashow, Michael F. ; Schemske, Douglas W. ; Oakley, Christopher G. ( November 2019 , American Journal of Botany)

   Despite myriad examples of local adaptation, the phenotypes and genetic variants underlying such adaptive differentiation are seldom known. Recent work on freezing tolerance and local adaptation in ecotypes ofArabidopsis thalianafrom Italy and Sweden provides an essential foundation for uncovering the genotype–phenotype–fitness map for an adaptive response to a key environmental stress.

   We examined the consequences of a naturally occurring loss‐of‐function (LOF) mutation in an Italian allele of the gene that encodes the transcription factorCBF2,which underlies a major freezing‐tolerance locus. We used four lines with a Swedish genetic background, each containing aLOFCBF2allele. Two lines had introgression segments containing the ItalianCBF2allele, and two contained deletions created usingCRISPR‐Cas9. We used a growth chamber experiment to quantify freezing tolerance and gene expression before and after cold acclimation.

   Freezing tolerance was lower in the Italian (11%) compared to the Swedish (72%) ecotype, and all four experimentalCBF2LOFlines had reduced freezing tolerance compared to the Swedish ecotype. Differential expression analyses identified 10 genes for which allCBF2LOFlines, and theITecotype had similar patterns of reduced cold responsive expression compared to theSWecotype.

   We identified 10 genes that are at least partially regulated byCBF2that may contribute to the differences in cold‐acclimated freezing tolerance between the Italian and Swedish ecotypes. These results provide novel insight into the molecular and physiological mechanisms connecting a naturally occurring sequence polymorphism to an adaptive response to freezing conditions.

    

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2. Ecological genetics of local adaptation in Arabidopsis : An 8‐year field experiment

   https://doi.org/10.1111/mec.17045  

   Oakley, Christopher G. ; Schemske, Douglas W. ; McKay, John K. ; Ågren, Jon ( June 2023 , Molecular Ecology)

   There is considerable evidence for local adaptation in nature, yet important questions remain regarding its genetic basis. How many loci are involved? What are their effect sizes? What is the relative importance of conditional neutrality versus genetic trade‐offs? Here we address these questions in the self‐pollinating, annual plantArabidopsis thaliana. We used 400 recombinant inbred lines (RILs) derived from two locally adapted populations in Italy and Sweden, grew the RILs and parents at the parental locations, and mapped quantitative trait loci (QTL) for mean fitness (fruits/seedling planted). We previously published results from the first 3 years of the study, and here add five additional years, providing a unique opportunity to assess how temporal variation in selection might affect QTL detection and classification. We found 10 adaptive and one maladaptive QTL in Italy, and six adaptive and four maladaptive QTL in Sweden. The discovery of maladaptive QTL at both sites suggests that even locally adapted populations are not always at their genotypic optimum. Mean effect sizes for adaptive QTL, 0.97 and 0.55 fruits in Italy and Sweden, respectively, were large relative to the mean fitness of the RILs (approximately 8 fruits/seedling planted at both sites). Both genetic trade‐offs (four cases) and conditional neutrality (seven cases) contribute to local adaptation in this system. The 8‐year dataset provided greater power to detect QTL and to estimate their locations compared to our previous 3‐year study, identifying one new genetic trade‐off and resolving one genetic trade‐off into two conditionally adaptive QTL.

    

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3. Distinct Cold Acclimation of Productivity Traits in Arabidopsis thaliana Ecotypes

   https://doi.org/10.3390/ijms23042129  

   Demmig-Adams, Barbara ; Polutchko, Stephanie K. ; Baker, Christopher R. ; Stewart, Jared J. ; Adams, William W. ( February 2022 , International Journal of Molecular Sciences)

   Improvement of crop climate resilience will require an understanding of whole-plant adaptation to specific local environments. This review places features of plant form and function related to photosynthetic productivity, as well as associated gene-expression patterns, into the context of the adaptation of Arabidopsis thaliana ecotypes to local environments with different climates in Sweden and Italy. The growth of plants under common cool conditions resulted in a proportionally greater emphasis on the maintenance of photosynthetic activity in the Swedish ecotype. This is compared to a greater emphasis on downregulation of light-harvesting antenna size and upregulation of a host of antioxidant enzymes in the Italian ecotype under these conditions. This differential response is discussed in the context of the climatic patterns of the ecotypes’ native habitats with substantial opportunity for photosynthetic productivity under mild temperatures in Italy but not in Sweden. The Swedish ecotype’s response is likened to pushing forward at full speed with productivity under low temperature versus the Italian ecotype’s response of staying safe from harm (maintaining redox homeostasis) while letting productivity decline when temperatures are transiently cold. It is concluded that either strategy can offer directions for the development of climate-resilient crops for specific locations of cultivation. 

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4. Thermal plasticity has higher fitness costs among thermally tolerant genotypes of Tigriopus californicus

   https://doi.org/10.1111/1365-2435.14568  

   Bogan, Samuel_N ; Porat, Olivia_I ; Meneses, Michael_J ; Hofmann, Gretchen_E ( May 2024 , Functional Ecology)

   Under climate change, ectotherms will likely face pressure to adapt to novel thermal environments by increasing their upper thermal tolerance and its plasticity, a measure of thermal acclimation. Ectotherm populations with high thermal tolerance are often less thermally plastic, a trade‐off hypothesized to result from (i) a phenotypic limit on thermal tolerance above which plasticity cannot further increase the trait, (ii) negative genetic correlation or (iii) fitness trade‐offs between the two traits. Whether each hypothesis causes negative associations between thermal tolerance and plasticity has implications for the evolution of each trait.

   We empirically tested the limit and trade‐off hypotheses by leveraging the experimental tractability and thermal biology of the intertidal copepodTigriopus californicus. Using populations from four latitudinally distributed sites in coastal California, six lines per population were reared under a laboratory common garden for two generations. Ninety‐six full sibling replicates (n = 4–5 per line) from a third generation were developmentally conditioned to 21.5 and 16.5°C until adulthood. We then measured the upper thermal tolerance and fecundity of sibships at each temperature.

   We detected a significant trade‐off in fecundity, a fitness corollary, between baseline thermal tolerance and its plasticity.Tigriopus californicuspopulations and genotypes with higher thermal tolerance were less thermally plastic. We detected negative directional selection on thermal plasticity under ambient temperature evidenced by reduced fecundity. These fitness costs of plasticity were significantly higher among thermally tolerant genotypes, consistent with the trade‐off hypothesis. This trade‐off was evident under ambient conditions, but not high temperature.

   Observed thermal plasticity and fecundity were best explained by a model incorporating both the limit and trade‐off hypotheses rather than models with parameters associated with one hypothesis. Effects of population and family on tolerance and plasticity negatively covaried, suggesting that a negative genetic correlation could not be ruled as contributing to negative associations between the traits. Our study provides a novel empirical test of the fitness trade‐off hypothesis that leverages a strong inference approach. We discuss our results' insights into how thermal adaptation may be constrained by physiological limits, genetic correlations, and fitness trade‐offs between thermal tolerance and its plasticity.

   Read the freePlain Language Summaryfor this article on the Journal blog.

    

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5. Fluctuating Environments Maintain Genetic Diversity through Neutral Fitness Effects and Balancing Selection

   https://doi.org/10.1093/molbev/msab173  

   Abdul-Rahman, Farah ; Tranchina, Daniel ; Gresham, David ( June 2021 , Molecular Biology and Evolution)

   Townsend, Jeffrey (Ed.)

   Abstract Genetic variation is the raw material upon which selection acts. The majority of environmental conditions change over time and therefore may result in variable selective effects. How temporally fluctuating environments impact the distribution of fitness effects and in turn population diversity is an unresolved question in evolutionary biology. Here, we employed continuous culturing using chemostats to establish environments that switch periodically between different nutrient limitations and compared the dynamics of selection to static conditions. We used the pooled Saccharomyces cerevisiae haploid gene deletion collection as a synthetic model for populations comprising thousands of unique genotypes. Using barcode sequencing, we find that static environments are uniquely characterized by a small number of high-fitness genotypes that rapidly dominate the population leading to dramatic decreases in genetic diversity. By contrast, fluctuating environments are enriched in genotypes with neutral fitness effects and an absence of extreme fitness genotypes contributing to the maintenance of genetic diversity. We also identified a unique class of genotypes whose frequencies oscillate sinusoidally with a period matching the environmental fluctuation. Oscillatory behavior corresponds to large differences in short-term fitness that are not observed across long timescales pointing to the importance of balancing selection in maintaining genetic diversity in fluctuating environments. Our results are consistent with a high degree of environmental specificity in the distribution of fitness effects and the combined effects of reduced and balancing selection in maintaining genetic diversity in the presence of variable selection. 

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