The scales and signatures of climate adaptation by theArabidopsistranscriptome

Abstract

Clines in allele frequency and trait variation can be highly informative for understanding how populations have historically adapted to climate variation across landscapes. However, as a consequence of the many complexities inherent to this process, these climate-associated differentiation patterns can be confounded, misleading, or obscured. Molecular phenotypes like gene expression levels are a potentially valuable means for resolving these complexities. Their intermediate position between genomes and organismal traits and their interrelatedness structured by gene regulatory networks can help parse how different climatic factors contribute to unique components of range-wide or region-specific diversity patterns. Here, we demonstrate these explanatory values of gene expression variation through integrative analyses of transcriptomic data from 665 Arabidopsis thaliana accessions. Differentiation of co-expressed genes is often associated with source site climate. Although some patterns hold range-wide, many other gene expression clines are specific to particular ancestry groups, reflecting how broad-scale and local combinations of selective agents differentially resolve functional interrelationships between plant defense, drought tolerance, and life history traits. We also extend these analyses to parse how different factors explain climate-associated variation in flowering time and its plasticity. Expression of key regulators FLC and SOC1 strongly predicts time to flower, consistent with previous work, but our results also highlight novel relationships that indicate as yet unexplored climate-related connections between defense signaling and flowering. Finally, we show that integrative models combining genotype and gene expression information predict variation in flowering time under ecologically realistic conditions more accurately than models based on either source alone.

Distinct signals of clinal and seasonal allele frequency change at eQTLs in Drosophila melanogaster

“…The levels of clinal enrichment observed are comparable to those observed for other functional categories in Drosophila (Machado et al 2016) and other species (Ye et al 2013;Mack et al 2018). Such an enrichment agrees with growing evidence that spatial differentiation at eQTLs contributes to local adaptation across taxa (Fraser 2013;Gould et al 2017;Mack et al 2018;Phifer-Rixey et al 2018;Kitano et al 2019;Colicchio et al 2020). We also show that the genome-wide enrichment signal is not driven by a few genes or solely due to linkage at a single locus (Figs.…”

“…Gene expression has been shown as an important driver of local adaptation (López-Maury et al 2008;Colicchio et al 2020). Consistent with the expectation that gene expression variation contributes to clinal adaptation (Adrion et al 2015), we show eQTLs are enriched for clinal SNPs (Fig.…”

“… 2008 ; Colicchio et al. 2020 ). Consistent with the expectation that gene expression variation contributes to clinal adaptation (Adrion et al.…”

“… 2019 ; Colicchio et al. 2020 ). We also show that the genome‐wide enrichment signal is not driven by a few genes or solely due to linkage at a single locus (Figs.…”

Unique signals of clinal and seasonal allele frequency change at eQTLs in Drosophila melanogaster

“…The levels of enrichment of clinal polymorphisms observed here are larger than those observed for other functional categories in Drosophila (Machado et al 2016) and other species (Ye et al 2013;Mack et al 2018), suggesting that SNPs underlying clinal adaptation are more likely to be eQTLs than other categories. This finding agrees with growing literature showing evidence that spatial differentiation at eQTLs contributes to local adaptation across various taxa (Fraser 2013;Gould et al 2017;Kitano et al 2018;Mack et al 2018;Phifer-Rixey et al 2018;Colicchio et al 2020).…”