Parallel and population-specific gene regulatory evolution in cold-adapted fly populations.

Area of Science:

• Evolutionary Biology
• Genomics
• Molecular Biology

Background:

• Gene regulatory changes are crucial for adaptive evolution.
• Limited studies have explored gene regulatory trait variation at a transcriptomic scale in natural populations.
• Understanding the characteristics of adaptive regulatory changes remains challenging.

Purpose of the Study:

• To investigate quantitative trait differentiation in gene expression and alternative splicing between natural Drosophila melanogaster populations.
• To examine evidence for parallel adaptive evolution in gene regulation across three independent cold tolerance evolution events.
• To differentiate the contributions of cis- and trans-regulation to adaptive evolution.

Main Methods:

• Assessed gene expression levels and alternative splicing (intron usage) in three pairs of cold-adapted and warm-adapted Drosophila melanogaster populations.
• Utilized population genetic data for single nucleotide polymorphism (SNP) level parallel evolution.
• Employed a flexible method to estimate cis- and trans-regulatory contributions to expression and splicing differences.

Main Results:

• Found evidence for parallel expression evolution between cold-adapted populations, with stronger parallelism in larval and adult stages compared to pupae.
• Observed substantial variation in the contributions of cis- and trans-regulation to adaptive evolution among population pairs.
• Identified cis-regulatory differences enriched among adaptation candidates and trans-regulatory differences implicated in parallel expression changes.

Conclusions:

• Cis-regulatory differences are frequently associated with local adaptation targets.
• Trans-regulatory differences are more likely involved in parallel expression changes during adaptation.
• This study enhances understanding of adaptive gene regulatory evolution and its inference in natural populations.