Comparative Genomic Insights into Adaptation, Selection Signatures, and Population Dynamics in Indigenous Indian Sheep and Foreign Breeds

Malarmathi Muthusamy¹Oludayo Michael Akinsola^1,2Pritam Pal³Chitra Ramasamy¹Saravanan Ramasamy¹Abdulraheem Arome Musa^4*Aranganoor Kannan Thiruvenkadan⁵

• ¹Department of Animal Genetics and Breeding, Veterinary College and Research Institute, TANUVAS, Namakkal, India
• ²Department of Theriogenology and Production, Faculty of Veterinary Medicine, University of Jos, Jos, Nigeria
• ³Animal Genetics and Breeding Division, Indian Council of Agricultural Research (ICAR)-National Dairy Research Institute (NDRI), Karnal, India
• ⁴Research Institute for Farm Animal Biology (FBN), Dummerstorf, Germany
• ⁵College of Poultry Production and Management, TANUVAS, Namakkal, India

India's indigenous sheep breeds have evolved under extreme and diverse agro-ecological pressures, yet the genomic basis of their resilience and local adaptation remains poorly understood. This study combines genomic inbreeding estimates, runs of homozygosity (ROH), population structure analyses, and composite selection scans to investigate three native Indian breeds-Changthangi, Deccani, and Garole-within a panel of nine breeds that also includes populations from Africa (Ethiopian Menz), East and South Asia (Tibetan, Chinese Merino, Bangladesh Garole, Bangladesh East), and Europe (Suffolk). ROH and heterozygosity estimates revealed strong contrasts: Bangladesh East sheep exhibited high genomic inbreeding (𝐹 𝑅𝑂𝐻 ≈ 14.4%) and low observed heterozygosity (~30.6%), whereas Deccani sheep showed low inbreeding (𝐹 𝑅𝑂𝐻 ≈ 1.1%) and high observed heterozygosity (~35.6%), consistent with broader gene flow and larger flock sizes. Changthangi and Garole showed moderate inbreeding and distinct ROH length profiles. Population structure analyses confirmed ecological clustering and gene flow shaped by geography and husbandry practices: high-altitude breeds clustered together, while directional migration edges traced admixture from European Suffolk into Changthangi and from Chinese Merino into Ethiopian Menz. Historical effective population sizes showed sharp declines in most breeds, especially those under recent selection. Selection scans identified 118 significant genomic regions across breeds. In Changthangi, key pathways included purinergic signaling, thyrotropin-releasing hormone, and autophagy-consistent with cold and hypoxia adaptation. Deccani showed enrichment for immune adhesion and epidermal regeneration, reflecting parasite resistance and heat stress. Garole displayed signals for gap-junction communication and skeletal development, aligned with high fertility and compact stature. These findings reveal ecotypespecific adaptive nature shaped by polygenic selection, gene flow, and demography, offering actionable insights for sustainable smallholder breeding strategies.