Gene expression clines reveal local adaptation and associated trade-offs at a continental scale

Abstract

Local adaptation, where fitness in one environment comes at a cost in another, should lead to spatial variation in trade-offs between life history traits and may be critical for population persistence. Recent studies have sought genomic signals of local adaptation, but often have been limited to laboratory populations representing two environmentally different locations of a species' distribution. We measured gene expression, as a proxy for fitness, in males of Drosophila subobscura, occupying a 20° latitudinal and 11 °C thermal range. Uniquely, we sampled six populations and studied both common garden and semi-natural responses to identify signals of local adaptation. We found contrasting patterns of investment: transcripts with expression positively correlated to latitude were enriched for metabolic processes, expressed across all tissues whereas negatively correlated transcripts were enriched for reproductive processes, expressed primarily in testes. When using only the end populations, to compare our results to previous studies, we found that locally adaptive patterns were obscured. While phenotypic trade-offs between metabolic and reproductive functions across widespread species are well-known, our results identify underlying genetic and tissue responses at a continental scale that may be responsible for this. This may contribute to understanding population persistence under environmental change.

Figure 1. Clinal expression in Drosophila subobscura populations along the European latitudinal transect.

(a,b) Distributions of correlation coefficients (Pearson’s r) between RNA-seq normalised reads and latitude for all the transcripts in the de novo transcriptome assembly (grey bars), putative testis-biased (red bars) and metabolic (blue bars) transcripts in six D. subobscura populations reared in two non-thermally stressful environmental conditions: lab common garden (a) and outdoor in situ (b). Positive r values denote transcripts with higher expression at higher latitudes, negative r values denote genes with higher expression at lower latitudes. The lab common garden and in situ datasets consist respectively of 15779 and 15947 total transcripts (grey bars), of which 1714 and 1680 are putative testis-biased (red bars) and 5257 and 5323 are metabolic homologs (blue bars). See Methods for how metabolic and testis-biased transcripts were classified. (c) Overlap between transcripts showing significant clinal expression (1%FDR, dashed lines in a,b) in the lab and in situ conditions; +CE = positive clinal expression, −CE = negative clinal expression.

Figure 2. Positive and negative clinally expressed genes in D. subobscura have marked tissue expression differences.

(a,b) Tissue expression profiles of significant clinally expressed genes in D. subobscura, estimated by using FlyAtlas expression data of D. melanogaster homologs. (c) tau (tissue specificity index) values associated with D. melanogaster homologs to D. subobscura clinally responding genes and de novo transcriptome assembly. tau values >0.9 are typical of genes having tissue-specific expression patterns.

Figure 3. Southern D. subobscura males invest more in copulation than northern males.

Copulation times of males from Valencia and Uppsala populations when crossed with females from the same or the alternative population.