Wolbachia in the Drosophila yakuba Complex: Pervasive Frequency Variation and Weak Cytoplasmic Incompatibility, but No Apparent Effect on Reproductive Isolation

Abstract

Three hybridizing species-the clade [(Drosophila yakuba, D. santomea), D. teissieri]-comprise the yakuba complex in the D. melanogaster subgroup. Their ranges overlap on Bioko and São Tomé, islands off west Africa. All three species are infected with Wolbachia-maternally inherited, endosymbiotic bacteria, best known for manipulating host reproduction to favor infected females. Previous analyses reported no cytoplasmic incompatibility (CI) in these species. However, we discovered that Wolbachia from each species cause intraspecific and interspecific CI. In D teissieri, analyses of F and backcross genotypes show that both host genotype and Wolbachia variation modulate CI intensity. Wolbachia-infected females seem largely protected from intraspecific and interspecific CI, irrespective of Wolbachia and host genotypes. Wolbachia do not affect host mating behavior or female fecundity, within or between species. The latter suggests little apparent effect of Wolbachia on premating or gametic reproductive isolation (RI) between host species. In nature, Wolbachia frequencies varied spatially for D. yakuba in 2009, with 76% (N = 155) infected on São Tomé, and only 3% (N = 36) infected on Bioko; frequencies also varied temporally in D. yakuba and D. santomea on São Tomé between 2009 and 2015. These temporal frequency fluctuations could generate asymmetries in interspecific mating success, and contribute to postzygotic RI. However, the fluctuations in Wolbachia frequencies that we observe also suggest that asymmetries are unlikely to persist. Finally, we address theoretical questions that our empirical findings raise about Wolbachia persistence when conditions fluctuate, and about the stable coexistence of Wolbachia and host variants that modulate Wolbachia effects.

Genome comparisons indicate recent transfer of wRi‐like Wolbachia between sister species Drosophila suzukii and D. subpulchrella

“…They are comparable to the experiments that inferred no CI associated with the native Wolbachia infections in D. yakuba , D. teissieri , and D. santomea (Charlat, Ballard, & Mercot, 2004; Zabalou et al., 2004). However, larger experiments by Cooper, Ginsberg, Turelli, and Matute (2017) revealed consistent, albeit weak, CI in all three yakuba clade species—and interspecific CI between these species. More replicated assays for CI in D. suzukii and D. subpulchrella , as well as investigation of whether CI is produced when w Spc and w Suz, are transinfected into CI‐expressing hosts such as D. simulans , will indicate whether the differences described in Table 6 are candidates for disrupting the molecular processes underlying CI (Beckmann et al., 2017; LePage et al., 2017).…”

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

“…This indicates that all hybrids were the F 1 sons of D. yakuba females and D. teissieri males [denoted F 1 (♀ yak × ♂ tei )]. Interestingly, the strength of reproductive isolation (RI) between reciprocal D. yakuba-D. teissieri crosses does not differ under standard laboratory conditions [11,12], leaving an open question about our inability to sample hybrids produced by D. teissieri females [denoted F 1 (♀ tei × ♂ yak )] on Bioko (see below).…”

“…Under standard laboratory conditions, non-ecological RI is equally strong between ♀ D. teissieri × ♂ D. yakuba and ♀ D. yakuba × ♂ D. teissieri crosses, and reciprocal hybrids do not differ in their survival rate [11,12,25]. This presents a conundrum; namely, what barriers might limit the prevalence and/or production of F 1 (♀ tei × ♂ yak ) hybrids in nature that are not revealed in the laboratory?…”

“…Both species are infected with maternally transmitted Wolbachia bacteria that cause weak cytoplasmic incompatibility (CI) when uninfected females mate with infected males. However, the strength of CI does not differ between reciprocal crosses, and Wolbachia seem to have no influence on RI in this clade [12], indicating that Wolbachia do not contribute to the paucity of F 1 (♀ tei × ♂ yak ) hybrids.…”

“…By measuring ecologically relevant phenotypes of D. yakuba , D. teissieri , and their hybrids in the lab and the field, our findings extend this knowledge to demonstrate temperature-dependent asymmetries in the strength of RI between reciprocal crosses. Notably, these two species also show other barriers to gene flow [11,12]. The role of biotic and abiotic conditions on facilitating hybridization and introgression remain largely understudied (but see [33]).…”