Rapid Global Spread of wRi-like Wolbachia across Multiple Drosophila

Abstract

Maternally transmitted Wolbachia, Spiroplasma, and Cardinium bacteria are common in insects [1], but their interspecific spread is poorly understood. Endosymbionts can spread rapidly within host species by manipulating host reproduction, as typified by the global spread of wRi Wolbachia observed in Drosophila simulans [2, 3]. However, because Wolbachia cannot survive outside host cells, spread between distantly related host species requires horizontal transfers that are presumably rare [4-7]. Here, we document spread of wRi-like Wolbachia among eight highly diverged Drosophila hosts (10-50 million years) over only about 14,000 years (5,000-27,000). Comparing 110 wRi-like genomes, we find ≤0.02% divergence from the wRi variant that spread rapidly through California populations of D. simulans. The hosts include both globally invasive species (D. simulans, D. suzukii, and D. ananassae) and narrowly distributed Australian endemics (D. anomalata and D. pandora) [8]. Phylogenetic analyses that include mtDNA genomes indicate introgressive transfer of wRi-like Wolbachia between closely related species D. ananassae, D. anomalata, and D. pandora but no horizontal transmission within species. Our analyses suggest D. ananassae as the Wolbachia source for the recent wRi invasion of D. simulans and D. suzukii as the source of Wolbachia in its sister species D. subpulchrella. Although six of these wRi-like variants cause strong cytoplasmic incompatibility, two cause no detectable reproductive effects, indicating that pervasive mutualistic effects [9, 10] complement the reproductive manipulations for which Wolbachia are best known. "Super spreader" variants like wRi may be particularly useful for controlling insect pests and vector-borne diseases with Wolbachia transinfections [11].

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

“…We also estimated a relative chronogram for the host species using the procedure implemented in Turelli et al. (). Our host phylogeny was based on the same 20 nuclear genes used in Turelli et al.…”

“…Our host phylogeny was based on the same 20 nuclear genes used in Turelli et al. (): aconitase, aldolase, bicoid, ebony, enolase, esc, g6pdh, glyp, glys, ninaE, pepck, pgi, pgm, pic, ptc, tpi, transaldolase, white, wingless , and yellow .…”

“…; Turelli et al. ). Wolbachia often manipulate host reproduction, inducing cytoplasmic incompatibility (CI) and male killing in Drosophila (Laven ; Yen and Barr ; Hoffmann et al.…”

“…Once they become sufficiently common, CI‐causing infections, such as w Ri‐like Wolbachia in Drosophila simulans and several other Drosophila (Turelli et al. ), spread to high equilibrium frequencies, dominated by a balance between CI and imperfect maternal transmission (Turelli and Hoffmann ; Kriesner et al. 2016).…”

The dynamics of preferential host switching: Host phylogeny as a key predictor of parasite distribution*

“…However, in some cases Wolbachia spread can be extremely rapid (Turelli et al. ). Overall, the Wolbachia– arthropod system is characterized by complex patterns of codiversification that differ between Wolbachia strains and host taxa and that we are only beginning to understand.…”