The ability to pass genetic material on to the next generation is a key driving factor of evolution, but the determinants of the evolution of reproductive fitness are relatively unknown. New genes have been shown to be essential for life in Drosophila melanogaster, but the extent to which new genes are important for reproductive fitness has not been thoroughly explored. We assessed the reproductive fitness effects of 91 newly evolved genes, with ages ranging from <1-25 million years, by carrying out constitutive knockdowns using RNAi for each gene in male and female Drosophila melanogaster. We quantified male fertilization success and female fecundity by counting and comparing the resulting offspring number from each set of knockdown reciprocal crosses to the reproductive output of non-knockdown parallel control crosses. Over half of the newly evolved genes (53%) we tested had significant beneficial effects on offspring number, revealing important roles of newly evolved genes in the reproductive fitness of Drosophila melanogaster. In addition, 7 new genes showed extreme effects on offspring number, resulting in near sterility when knocked down, suggesting a handful of new genes are essential for normal Drosophila melanogaster fertility.
Overall, 47% of the new genes tested had a significant beneficial effect on male reproductive fitness compared to the controls, while only 5 new genes had a significant beneficial effects on female offspring number (one gene had a significant beneficial effect for both sexes), revealing differential fitness effects of new genes in males and females. 20% of the new genes had significant differential effects of the same gene on offspring number between males and females; in the majority of these cases (83%), the new gene was significantly beneficial to male reproductive success, whereas it did not significantly affect the female offspring number. Expression data revealed that the majority of new genes were highly expressed in the testis and male accessory gland, providing additional evidence for the role of new genes in male reproductive fitness. Male and female adaptive needs are often different, due to their unique reproductive roles. Our results support the idea that new genes are a driving force in the evolution of reproductive fitness and male-driven evolution is an important component contributing to the retention of new genes in the Drosophila melanogaster genome.