Comprehensive Analysis of 122 Guinea Fowl Genomes Across Three Continents Delineates Their Domestication and Evolutionary Patterns with Special Reference to India

Abstract

The guinea fowl (Numida meleagris), a thermo-tolerant and disease-resilient poultry species, holds great potential for sustainable poultry production in climate-vulnerable regions. The genomic aspects of this species remain largely understudied. The present study aims to delineate the patterns of domestication and understand the evolutionary dynamics of guinea fowl populations (wild and domestic) across three continents, utilizing whole-genome sequencing data from 122 genomes. The population structure analyses (ADMIXTURE, PCA, phylogeny, FST, LD, and MAF) revealed that Indian guinea fowl (CARI) shared close ancestry with Iranian (IRAD) and Chinese (CHID) domesticated populations while remaining distinct from wild lineages. The runs of homozygosity (ROH) identified 49,088 segments, with short fragments (ROHs) preponderant in Indian and domestic populations, reflecting historical inbreeding and effects of domestication cum selection. Copy number variation (CNV) analysis revealed 105,178 CNVs concatenated into 40,067 CNV regions (CNVRs) across 11 populations, establishing the first CNV atlas for guinea fowl at the global level. Gene annotation of overlapping ROH and CNVRs revealed 1080 common candidates across Asian guinea fowl populations, i.e., the Indian guinea fowl (CARI), IRAD, and CHID, including FOS, EPAS1, CD74, and CSF1R. These genes have earlier been associated with immune regulation, stress response, and thermal adaptation. Selection signature scans, integrating intra-population (iHS) and inter-population (XP-EHH) approaches, uncovered genes under positive selection linked to immune response (like BCL11B, IL18, and GPC3), thermo-tolerance (like TRPV4 and BAG3), lipid metabolism (like AACS and ELOVL4), and pigmentation (BCO2). These signatures highlight the molecular basis of resilience in guinea fowl and their potential to withstand climate-induced stresses. This study presents the first global CNV atlas for guinea fowl and provides the first comprehensive genomic characterization of the Indian domestic population, integrating ROH, CNV, and selection signature analyses. It offers a comprehensive assessment of guinea fowl genomes (wild and domesticated) across three continents, offering insights into domestication, evolutionary dynamics, and the genetic basis of their adaptation and resilience.