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

Abstract

Maternally transmitted Wolbachia bacteria infect about half of all insect species. They usually show imperfect maternal transmission and often produce cytoplasmic incompatibility (CI). Irrespective of CI, Wolbachia frequencies tend to increase when rare only if they benefit host fitness. Several Wolbachia, including wMel that infects Drosophila melanogaster cause weak or no CI and persist at intermediate frequencies. On the island of São Tomé off West Africa, the frequencies of wMel-like Wolbachia infecting D. yakuba (wYak) and D. santomea (wSan) fluctuate, and the contributions of imperfect maternal transmission, fitness effects, and CI to these fluctuations are unknown. We demonstrate spatial variation in wYak frequency and transmission on São Tomé. Concurrent field estimates of imperfect maternal transmission do not predict spatial variation in wYak frequencies, which are highest at high altitudes where maternal transmission is the most imperfect. Genomic and genetic analyses provide little support for D. yakuba effects on wYak transmission. Instead, rearing at cool temperatures reduces wYak titer and increases imperfect transmission to levels observed on São Tomé. Using mathematical models of Wolbachia frequency dynamics and equilibria, we infer temporally variable imperfect transmission or spatially variable effects on host fitness and reproduction are required to explain wYak frequencies. In contrast, spatially stable wSan frequencies are plausibly explained by imperfect transmission, modest fitness effects, and weak CI. Our results provide insight into causes of wMel-like frequency variation in divergent hosts. Understanding this variation is crucial to explain Wolbachia spread and to improve wMel biocontrol of human disease in transinfected mosquito systems.

Pervasive Effects ofWolbachiaon Host Temperature Preference

“…Our results add to mounting literature showing that temperature is an important abiotic factor mediating interactions between Wolbachia and their hosts (112). Wolbachia titer seems to be especially sensitive to temperature (42,58,60,61,63,(113)(114)(115)(116). Our 24-h temperature shift experiments suggest that Wolbachia titer can change over very short time periods due to environmental conditions.…”

“…Increased Wolbachia titer in males is unlikely to affect rates of maternal Wolbachia transmission, but perhaps temperature-associated titer increases could alter the strength of cytoplasmic incompatibility caused by males infected with wSh or wTei (85,87,95,106). Other studies have also reported male-biased effects on Wolbachia titer (42,62,107); for example, our own work demonstrated that maternal transmission of wYak to sons is more efficient than to daughters when D. yakuba mothers are reared in cold 20°C conditions (42).…”

“…For example, exposure to heat stress is associated with correlated declines in Wolbachia titer and the severity of cytoplasmic incompatibility in wMel-transinfected mosquitoes (60,61). In Drosophila hosts, temperature has been shown to modify the strength of cytoplasmic incompatibility (37,58,94,117), maternal transmission (42,110), and host fitness effects (118)(119)(120). Clearly, more work on how temperature influences Wolbachia-host interactions is needed.…”

“…The fitness consequences of Wolbachia in host tissues ultimately determine infection spread, and initial spread from low frequencies requires positive Wolbachia effects on host fitness (36)(37)(38). Exactly how Wolbachia alters components of host fitness is poorly understood (39), even though theoretical and population-level analyses indicate pervasive positive effects on host fitness (1,31,37,(40)(41)(42).…”

“…Differences in T p between infected and uninfected flies could arise from conflicting physiological requirements of Wolbachia and their hosts. Wolbachia titer in host bodies is sensitive to temperature fluctuations (57), such that exceedingly cool (Ͻ20°C) and warm (Ͼ25°C) temperatures can reduce titer and the efficiency of maternal Wolbachia transmission (42,(57)(58)(59)(60)(61)(62)(63). Wolbachia-induced changes to T p could provide more favorable thermal conditions for bacterial replication in hosts.…”