Genome regions that are highly conserved between distantly-related organisms are assumed to have important fitness effects that have been preserved by natural selection over long periods of time. This assumption has led to two others: 1) the evolution of important genome regions is slow and 2) new genome regions do not have significant fitness effects. However, new genetic variants are precisely those that cause individuals to vary and thus drive evolution. A complete understanding of how and how rapidly genomes and fitnesses change thus depends on characterization of the evolutionary forces that act on and the fitness effects of new variants.
We investigated these characteristics of a set of 27 Drosophila melanogaster-specific genes. These genes were formed by duplication and fixed after D. melanogaster and D. simulans diverged (~2 mya). We screened 12 D. melanogaster-specific genes for severe fitness and morphological defects using available mutants and RNA interference (RNAi). Specific and constitutive expression knockdown of 4/12 genes is lethal. That is, significantly fewer (1 gene) or no (3 genes) RNAi flies survive to adulthood. Thus, 1/3 genes rapidly acquired a critical fitness effect. Natural selection appears to have dominated this process, as 50% of D. melanogaster-specific genes reside in regions with extremely negative Tajima’s D and/or Fay and Wu’s H statistics. These findings suggest that D. melanogaster-specific genes were subject to recent and strong selection, and are supported by comparisons of polymorphism and divergence in the surrounding regions. While D. melanogaster-specific genes exhibit few signatures of rapid sequence evolution, 37% have accumulated insertion/deletions, recruited additional amino acids, or are chimeric relative to their parent copies. In addition, duplicate pairs rapidly diverged in expression patterns across tissues and developmental times.
We thus provide direct and indirect evidence that D. melanogaster-specific genes can rapidly evolve significant fitness effects. Our results support a model in which 1) new genes become distinct from their parents concurrent with their formation, 2) selection immediately acts on new genes to drive them to fixation or purge them from the population, and 3) new gene function and fitness effects are refined during and after fixation. These findings suggest that new genes can play important roles in determining organismal fitness shortly after they are formed and that importance does not require long-term conservation.