Predicted deleterious mutations reveal the genetic architecture of male reproductive success in a lekking bird

Deleterious mutations are ubiquitous in natural populations and, when expressed, reduce fitness. However, the specific nature of these mutations and the ways in which they impact fitness remain poorly understood. We exploited recent advances in genomics to predict deleterious mutations in the black grouse (Lyrurus tetrix), an iconic lekking species. Analysis of 190 whole genomes alongside comprehensive life-history data including repeated measures of behavioural, ornamental and fitness traits revealed that deleterious mutations identified through evolutionary conservation and functional prediction are associated with reduced male lifetime mating success. Both homozygous and heterozygous deleterious mutations reduce fitness, indicating that fully and partially recessive mutations contribute towards an individual’s realized mutation load. Notably, deleterious mutations in promotors have disproportionally negative fitness effects, suggesting that they impair an individual’s ability to dynamically adjust gene expression to meet context-dependent functional demands. Finally, deleterious mutations impact male mating success by reducing lek attendance rather than by altering the expression of ornamental traits, suggesting that behaviour serves as an honest indicator of genetic quality. These findings offer insights into the genetic architecture of male fitness and illuminate the complex interplay between genetic variation and phenotypic expression. Analysis of whole genomes and life-history data of male black grouse shows that deleterious mutations, especially those in promotors, reduce lifetime reproductive success.