Decoupled differentiation of gene expression and coding sequence among Drosophila populations

Area of Science:

• Evolutionary biology
• Genomics
• Population genetics

Background:

• The link between genetic variation and phenotypic differences across populations is crucial for evolutionary studies.
• While genotype-phenotype correlations are often poor, gene expression is increasingly used as a proxy for phenotype in the genomic era.
• The relationship between population-level gene expression differentiation and genetic marker differentiation is largely unexplored.

Purpose of the Study:

• To investigate the correlation between population differentiation in gene expression and nucleotide sequence polymorphism.
• To explore the role of cis-regulatory regions versus coding sequences in driving gene expression differences.
• To understand the evolutionary forces (selection vs. drift) shaping gene expression and sequence variation.

Main Methods:

• Analysis of gene expression and nucleotide sequence polymorphism for 106 genes in Drosophila melanogaster strains from two mating races (Cosmopolitan and Zimbabwe).
• Quantification of population differentiation for gene expression (QST) and coding sequences (GST).
• Exploratory analysis of GST in 5' flanking sequences and its correlation with QST.

Main Results:

• Differentiation in gene expression (QST) and coding sequences (GST) were uncorrelated, with QST generally exceeding GST.
• Differentiation in 5' flanking sequences (GST) correlated with gene expression differentiation (QST), unlike coding sequences.
• Evidence suggests selection acts on global gene expression levels, but 5' sequence polymorphisms appear selectively neutral.

Conclusions:

• Population differentiation in cis-regulatory regions is decoupled from differentiation in coding regions.
• Selection may target higher organizational levels of gene expression regulation rather than specific nucleotide sequences.
• Identifying the precise nucleotide targets of selection for phenotypic evolution, particularly in gene expression, remains challenging.