Environmental and Genetic Contributions to Imperfect w Mel-Like Wolbachia Transmission and Frequency Variation

Maternally transmittedWolbachiabacteria infect about half of all insect species. They usually show imperfect maternal transmission and often produce cytoplasmic incompatibility (CI). Irrespective of CI,Wolbachiafrequencies tend to increase when rare only if they benefit host fitness. SeveralWolbachia, includingwMel that infectsDrosophila melanogaster, cause weak or no CI and persist at intermediate frequencies. On the island of Sao Tome off West Africa, the frequencies ofwMel-likeWolbachiainfectingDrosophila yakuba(wYak) andDrosophila santomea(wSan) fluctuate, and the contributions of imperfect maternal transmission, fitness effects, and CI to these fluctuations are unknown. We demonstrate spatial variation inwYak frequency and transmission on Sao Tome. Concurrent field estimates of imperfect maternal transmission do not predict spatial variation inwYak frequencies, which are highest at high altitudes where maternal transmission is the most imperfect. Genomic and genetic analyses provide little support forD. yakubaeffects onwYak transmission. Instead, rearing at cool temperatures reduceswYak titer and increases imperfect transmission to levels observed on Sao Tome. Using mathematical models ofWolbachiafrequency dynamics and equilibria, we infer that temporally variable imperfect transmission or spatially variable effects on host fitness and reproduction are required to explainwYak frequencies. In contrast, spatially stablewSan frequencies are plausibly explained by imperfect transmission, modest fitness effects, and weak CI. Our results provide insight into causes ofwMel-like frequency variation in divergent hosts. Understanding this variation is crucial to explainWolbachiaspread and to improvewMel biocontrol of human disease in transinfected mosquito systems.