A maladaptive combination of traits contributes to the maintenance of a stable hybrid zone between two divergent species of Drosophila

Abstract

ABSTRACTGeographical areas where two species come into contact and hybridize serve as natural laboratories for assessing mechanisms that limit gene flow between species. The ranges of about half of all closely related Drosophila species overlap, and the genomes of several pairs reveal signatures of past introgression. However, only two contemporary hybrid zones have been characterized in the genus, and both are recently diverged sister species (D. simulans-D. sechellia, Ks = 0.05; D. yakuba-D. santomea, Ks = 0.048). Here we present evidence of a new hybrid zone, and the ecological mechanisms that maintain it, between two highly divergent Drosophila species (Ks = 0.11). On the island of Bioko in west Africa, D. teissieri occupies mostly forests, D. yakuba occupies mostly open agricultural areas, and recently, we discovered that hybrids between these species occur near the interface of these habitats. Genome sequencing revealed that all field-sampled hybrids are F1 progeny of D. yakuba females and D. teissieri males. We found no evidence for either advanced-generation hybrids or F1 hybrids produced by D. teissieri females and D.yakuba males. The lack of advanced-generation hybrids on Bioko is consistent with mark-recapture and laboratory experiments that we conducted, which indicate hybrids have a maladaptive combination of traits. Like D. yakuba, hybrids behaviorally prefer open habitat that is relatively warm and dry, but like D. teissieri, hybrids have low desiccation tolerance, which we predict leaves them physiologically ill-equipped to cope with their preferred habitat. These observations are consistent with recent findings of limited introgression in the D. yakuba clade and identify an ecological mechanism for limiting gene flow between D. yakuba and D. teissieri; namely, selection against hybrids that we have documented, in combination with hybrid male sterility, contributes to the maintenance of this narrow (~30m), stable hybrid zone centered on the forest-open habitat ecotone. Our results show how a deleterious combination of parental traits can result in unfit or maladapted hybrids.