The Unit of Selection in DROSOPHILA MERCATORUM. II. Genetic Revolution and the Origin of Coadapted Genomes in Parthenogenetic Strains

Abstract

Drosophila mercatorum is a sexual species that can reproduce parthenogenetically. Previous studies revealed that parthenogenetic strains had "coadapted genomes" with high fitness under parthenogenesis and total homozygosity due to nonadditive and nonmultiplicative fitness interactions between chromosomal segments scattered throughout the genome. To study the evolutionary origins of such coadapted genomes, females from sexual matings in nature were isolated as virgins and challenged to reproduce parthenogenetically. Fitness studies were performed on genomes derived from these sexual females and upon their successful parthenogenetic progeny. By straddling the reproductive transition from sex to parthenogenesis, these fitness studies demonstrated that coadapted genomes arise immediately, apparently due to an intense selective bottleneck accompanying the reproductive transition, and are not due to the slow accumulation of epistatic complexes via mutation after parthenogenesis has already been established. The reproductive transition may also serve as an experimental model of the "genetic revolution" theory of speciation because the transition involves (1) the ultimate founder effect (one genome), (2) maximal genetic drift and fixation, (3) a drastic change in genetic environment characterized by total homozygosity, and (4) an intense selective bottleneck that interacts with the change in genetic environment and the need to adapt to a laboratory environment and a novel system of reproduction. Thus, all the elements theorized to underlie genetic revolution are present, albeit in extreme form. This study indicates that genetic revolutions are real phenomena that can quickly alter morphology, development, life history parameters and behavior. Indeed, the alterations can be so drastic that a new "species" evolves, complete with pre- and post-mating isolating mechanisms. However, isozyme loci do not appear to be the target of this genetic revolution, but rather loci regulating fundamental developmental processes. However, isozyme loci may be useful in predicting the a priori chance of a successful revolution since they can indicate how the population structure of the parent population influences levels of individual heterozygosity, the prime source of the genetic variability in the founder population that must pass through the selective bottleneck.