A Maladaptive Combination of Traits Contributes to the Maintenance of a Drosophila Hybrid Zone

Drosophila teissieri and D. yakuba diverged approximately 3 mya and are thought to share a large, ancestral, African range [1–3]. These species now co-occur in parts of continental Africa and in west Africa on the island of Bioko [1, 4]. While D. yakuba is a human commensal, D. teissieri seems to be associated with Parinari fruits, restricting its range to forests [4–6]. Genome data indicate introgression, despite no evidence of contemporary hybridization. Here we report the discovery of D. yakuba-D. teissieri hybrids at the interface of secondary forests and disturbed, open habitats on Bioko. We demonstrate that hybrids are the F₁ progeny of D. yakuba females and D. teissieri males. At high temperatures like those found on Bioko, D. teissieri females are generally less receptive to mating, and in combination with temperature effects on egg lay and egg-to-adult viability, this decreases the potential for gene flow between female D. teissieri and male D. yakuba relative to the reciprocal cross. Field and laboratory experiments demonstrate that F₁ hybrids have a maladaptive combination of D. yakuba behavior and D. teissieri physiology, generating additional barriers to gene flow. Nevertheless, analysis of introgressed and non-introgressed regions of the genome indicate that, while rare, gene flow is relatively recent. Our observations identify precise intrinsic and extrinsic factors that, along with hybrid male sterility, limit gene flow and maintain these species. These data contribute to a growing body of literature that suggests the Gulf of Guinea may be a hotspot for hybridization. Cooper et al. document hybridization between Drosophila yakuba and D. teissieri on Bioko in west Africa. Temperature-dependent reproductive isolation limits the production of hybrids produced by D. teissieri females. A maladaptive combination of D. yakuba behavior and D. teissieri physiology in hybrids generates additional barriers to gene flow.