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

Abstract

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 F 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 F 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.

Loss of cytoplasmic incompatibility and minimal fecundity effects explain relatively lowWolbachiafrequencies inDrosophila mauritiana

“…This is surely many thousands of generations given previous estimates that consider the temperature dependence of Drosophila development (Cooper et al. , ). As shown by our mathematical analyses (Eq.…”

Introgressive and horizontal acquisition of Wolbachia byDrosophila yakuba-clade hosts and horizontal transfer of incompatibility loci between distantly related Wolbachia

“…2018). The ranges of D. yakuba and D. teissieri overlap throughout continental Africa, but contemporary hybridization has not been observed outside of Bioko (Cooper et al . 2018).…”

“…2006; Llopart et al . 2014; Turissini and Matute 2017; Cooper et al . 2018), and the Wolbachia infecting all three species ( w San, w Tei, and w Yak) are at intermediate frequencies and identical with respect to commonly used typing loci (Lachaise et al .…”

Vocal divergence is concordant with genomic evidence for strong reproductive isolation in grasshopper mice (Onychomys)

“…Behavioral divergence is considered to be a major factor driving the evolution of reproductive barriers (Mayr, 1963;Turissini, McGirr, Patel, David, & Matute, 2017;West-Eberhard, 1983). However, recent studies of speciation using next-generation sequencing indicate substantial gene flow between closely related taxa despite strong intrinsic and/or extrinsic costs to hybridization (e.g., Cooper, Sedghifar, Nash, Comeault, & Matute, 2018;Rafati et al, 2018;Souissi, Bonhomme, Manchado, Bahri-Sfar, & Gagnaire, 2018). Such findings emphasize the importance of understanding the behavioral mechanisms underlying assortative mating in determining the permeability of species boundaries upon secondary contact (Kopp et al, 2018).…”