The interplay between epigenomic and transcriptomic variation during ecotype divergence in stickleback

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Abstract
Populations colonizing contrasting environments are likely to undergo adaptive divergence and evolve ecotypes with locally adapted phenotypes. While diverse molecular mechanisms underlying ecotype divergence have been identified, less is known about their interplay and degree of divergence. Here we integrated epigenomic and transcriptomic data to explore the interactions among gene expression, alternative splicing, DNA methylation, and microRNA expression to gauge the extent to which patterns of divergence at the four molecular levels are aligned in a case of postglacial divergence between marine and freshwater ecotypes of nine-spined sticklebacks (Pungitius pungitius). Despite significant genome-wide associations between epigenomic and transcriptomic variation, we found largely non-parallel patterns of ecotype divergence across epigenomic and transcriptomic levels, with predominantly nonoverlapping (ranging from 43.40 to 87.98%) sets of differentially expressed, spliced and methylated genes, and candidate genes targeted by differentially expressed miRNA between the ecotypes. Furthermore, we found significant variation in the extent of ecotype divergence across different molecular mechanisms, with differential methylation and differential splicing showing the highest and lowest extent of divergence between ecotypes, respectively. Finally, we found a significant enrichment of genes associated with ecotype divergence in differential methylation. Our results suggest a nuanced relationship between epigenomic and transcriptomic processes, with alignment at the genome-wide level masking relatively independent effects of different molecular mechanisms on ecotype divergence at the gene level.
Funding Information
  • Research Council of Finland (129662, 134728 and 218343)
  • NSERC Discovery Grant and Canada Research Chair
  • National Natural Science Foundation of China (32161160321, 31672273 and 32022009, 32170417)
  • Shanghai Sailing Program (21YF1403200)

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