Linked selection of insertions and deletions in coding regions of the great tit genome

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Abstract

Insertions and deletions (indels) are a ubiquitous form of genomic variation; yet, their contribution to adaptive evolution remains poorly understood. Technical challenges in identifying indels and integrating them into existing evolutionary models have limited their study, but previous work suggests that they may be subject to strong selective pressures. Here, we investigated selective signatures of indels in coding regions of the great tit ( Parus major ). We identified species-specific indels in protein-coding genes and analyzed the 300 bp flanking regions of indels using codeml to estimate dN, dS, and ω (dN/dS). Additionally, we performed enrichment analyses and protein structure modeling to assess functional consequences. We found that mutations in the flanking regions of indels are non-random and that selection strength varies with indel type and length. Genes including indels were enriched for functions related to protein and nucleic acid binding and linked to potentially adaptive traits such as vocal learning, migration, circadian rhythm, and environmental acclimation. Our results suggest that insertions and deletions may serve as hotspots of selection, influencing nearby sequences and contributing to adaptation in the great tit.

Significance Statement

Small DNA changes called insertions and deletions (indels) are common in genomes, but their role in evolution is often overlooked because they are difficult to study. Using the genome of the great tit, a well-studied songbird, we identified thousands of indels in protein-coding regions and examined how they affect nearby DNA. We found that indels are not neutral accidents: they show signs of natural selection and may influence important traits. Some of the affected genes are linked to behaviors and adaptations that are crucial for survival, such as vocal learning, migration, and adaptation to new environments. These results suggest that indels can act as hotspots for evolutionary change and may help explain how species adapt to their surroundings. By high-lighting the evolutionary importance of these often-neglected mutations, our study opens new perspectives on the genetic basis of adaptation.

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