Coevolution of male and female reproductive traits drive cascading reinforcement inDrosophila yakuba

ABSTRACT When the ranges of two hybridizing species overlap, individuals may ‘waste’ gametes on inviable or infertile hybrids. In these cases, selection against maladaptive hybridization can lead to the evolution of enhanced reproductive isolation in a process called reinforcement. On the slopes of the African island of São Tomé, Drosophila yakuba and its endemic sister species D. santomea have a well-defined hybrid zone. Drosophila yakuba females from within this zone show increased postmating-prezygotic isolation towards D. santomea males when compared with D. yakuba females from allopatric populations. To understand why reinforced gametic isolation is confined to areas of secondary contact and has not spread throughout the entire D. yakuba geographic range, we studied the costs of reinforcement in D. yakuba using a combination of natural collections and experimental evolution. We found that D. yakuba males from sympatric populations sire fewer progeny than allopatric males when mated to allopatric D. yakuba females. Our results suggest that the correlated evolution of male and female reproductive traits in sympatric D. yakuba have associated costs (i.e., reduced male fertility) that prevent the alleles responsible for enhanced isolation from spreading outside the hybrid zone.