Increased Genetic Load in Breed Chickens and Reduced Coding Content in Long ROH

Domestic organisms provide valuable models for studying the impact of population bottlenecks, inbreeding, and artificial selection on the accumulation of deleterious variants. While previous studies largely focused on coding variants, our study investigated both coding and noncoding contributions to genetic load in diverse chicken breeds, revealing the consequences of inbreeding and artificial selection on genome-wide patterns of deleterious variation. Using representative chicken populations with different selection histories, we show that domestication processes significantly impact the genetic load in chicken populations. Village chickens, which have experienced only the initial domestication, exhibit comparable levels of neutral heterozygosity and realized load to their wild progenitor, the Red Jungle Fowl. In contrast, breed chickens that have undergone more intense artificial selection show a significant decrease in neutral heterozygosity, an increase in the ratio of 0-fold to 4-fold heterozygosity, and a higher realized genetic load in both coding and noncoding regions. However, signals of purging of loss-of-function and noncoding deleterious variants were also detected in domestic chicken. Inbreeding is a major contributor to the increase in genome-wide realized load. We found selection against recently inbred individuals carrying long ROHs covering more coding regions, and an enrichment of homozygous noncoding deleterious variants in ROHs of no less than 2 Mb. Additionally, we found that artificial selection drastically elevated the relative allele frequency of deleterious variants within sweep regions. These findings have implications for the importance of genetic background evaluation of breeding flocks and strategic management to maintain long-term health in domestic populations.