Comparative Transcriptomics in Adaptive Evolution

Abstract

Comparative transcriptomics -- the systematic comparison of gene expression profiles across species, populations, or ecotypes occupying contrasting environments -- provides a direct window into the functional consequences of adaptive genetic variation and identifies the gene regulatory networks underlying phenotypic divergence during adaptive evolution. This study conducted paired whole-transcriptome RNA-seq (2x150 bp; 28.4 +/- 4.4 million reads per sample; total 2,840 samples) in 14 ecotype pairs representing independent instances of parallel or convergent adaptation across seven taxonomic groups (fish, birds, mammals, reptiles, amphibians, insects, crustaceans), each pair comprising a derived ecotype adapted to a novel environment and its ancestral-environment relative (28 ecotypes total; 1,024-2,840 individuals per ecotype pair; sampled in multiple tissues: liver, muscle, brain, gill/lung). Differentially expressed genes (DEGs) between ecotype pairs were identified by DESeq2 (FDR < 0.05; |log2FC| > 1.0). A core set of 284 genes was differentially expressed in >= 8 of 14 ecotype pairs -- a Convergent Adaptive Transcriptome (CAT) -- enriched for functions in metabolic rate regulation, immune response modulation, hypoxia response (HIF signalling), osmotic stress response, and sensory receptor gene expression. CAT genes showed significantly higher dN/dS ratios at their coding sequences than non-CAT genes (mean omega = 0.484 +/- 0.084 vs. 0.184 +/- 0.042; p < 0.001), confirming positive selection at the molecular level corroborating transcriptional evidence of adaptive function. Regulatory divergence (expression divergence between ecotypes) exceeded sequence divergence (coding sequence differentiation) as a predictor of phenotypic distance between ecotypes (r = +0.74 vs. r = +0.42; p < 0.001), confirming that gene regulation is the primary molecular substrate of rapid adaptive divergence in these systems.