Genome-wide associations of fitness components reveal antagonistic pleiotropy and sexual conflict in the Florida Scrub-Jay

Abstract

Natural populations often exhibit substantial genetic variation in fitness-related traits, providing the raw material for adaptation. The persistence of high levels of genetic variation in the presence of genetic drift and directional selection has long puzzled evolutionary biologists1-3. Recent studies suggest that antagonistic pleiotropy may play a greater role than previously appreciated, highlighting the need for more empirical studies that consider both sexual antagonism and life-history trade-offs4. Here, we performed a comprehensive assessment of fitness trade-offs within and between sexes in an extensively monitored natural population of Florida Scrub-Jays (Aphelocoma coerulescens)5. We found significant additive genetic variance for female fitness and identified several loci associated with variation in survival, fecundity, and lifetime reproductive success. Many loci associated with multiple fitness components had antagonistic effects, particularly within males. Considering genome-wide polygenic effects, we found multiple genetic trade-offs both within and between sexes, especially when considering different fitness components between sexes. Comparing allele frequency trajectories for putatively pleiotropic loci demonstrated that antagonistic SNPs had smaller allele frequency changes than concordant SNPs. Our fine-scale dissection of fitness components reveals substantial antagonistic pleiotropy that affects short-term evolution, highlighting the importance of antagonistic selection in maintaining genetic variation over short time scales in nature.