Additivity of the genetic load is a product of both synergistic and antagonistic epistasis in Drosophila

Epistasis has been theoretically implicated in several major evolutionary processes, including the evolution of sex and speciation, but empirical evidence for its impact is still lacking. We tested for epistatic interactions using a full-sib inbreeding design in Drosophila melanogaster . We examined the effects of deleterious mutations on two sequential components of life-history: pupal productivity and pupa-to-adult viability. We observed an accelerating decline in pupal productivity with increasing inbreeding coefficient, consistent with synergistic epistasis, whereas pupa-to-adult viability exhibited a decelerating decline, consistent with antagonistic epistasis. This decoupling led to an overall linear decline in the production of adult offspring with increasing inbreeding. Our findings suggest that epistatic interactions can be highly trait-specific, underscoring the importance of analyzing individual, physiologically interconnected, fitness traits to understand the role of epistasis in evolutionary processes.