Stable coexistence of incompatible Wolbachia along a narrow contact zone in mosquito field populations

Abstract

In arthropods, the intracellular bacteria Wolbachia often induce cytoplasmic incompatibility (CI) between sperm and egg, which causes conditional embryonic death and promotes the spatial spread of Wolbachia infections into host populations. The ability of Wolbachia to spread in natural populations through CI has attracted attention for using these bacteria in vector-borne disease control. The dynamics of incompatible Wolbachia infections have been deeply investigated theoretically, whereas in natural populations, there are only few examples described, especially among incompatible infected hosts. Here, we have surveyed the distribution of two molecular Wolbachia strains (wPip11 and wPip31) infecting the mosquito Culex pipiens in Tunisia. We delineated a clear spatial structure of both infections, with a sharp contact zone separating their distribution areas. Crossing experiments with isofemale lines from different localities showed three crossing types: wPip11-infected males always sterilize wPip31-infected females; however, while most wPip31-infected males were compatible with wPip11-infected females, a few completely sterilize them. The wPip11 strain was thus expected to spread, but temporal dynamics over 7 years of monitoring shows the stability of the contact zone. We examined which factors may contribute to the observed stability, both theoretically and empirically. Population cage experiments, field samples and modelling did not support significant impacts of local adaptation or assortative mating on the stability of wPip infection structure. By contrast, low dispersal probability and metapopulation dynamics in the host Cx. pipiens probably play major roles. This study highlights the need of understanding CI dynamics in natural populations to design effective and sustainable Wolbachia-based control strategies.

The Bacteriome of Bat Flies (Nycteribiidae) from the Malagasy Region: a Community Shaped by Host Ecology, Bacterial Transmission Mode, and Host-Vector Specificity

“…Facultative association between nycteribiid Wolbachia suggests that their interaction over evolutionary history is more recent than that of the ALOs despite the fact that fluorescence in situ hybridization-based physiological studies suggest a common mechanism of vertical transmission for all nycteribiid bacterial endosymbionts (13). This is in keeping with observations in other arthropod species, where Wolbachia strains are seen to have complex phylogenetic histories due to their dual capacity to form stable coexisting mixed populations within arthropod communities (54,55) and to invade entire populations by manipulating host reproduction (56). While the potential of Wolbachia to manipulate the reproduction of bat flies is unknown, it is interesting to note that a recent study observed biased sex ratios in bat fly populations (Trichobius frequens) in Puerto Rico (57).…”

First report of the endobacteriaWolbachiain natural populations ofCulex pipiensin Morocco

“…2) Marrakech may be considered as a sympatric zone where close contact between populations of Cx. pipiens infected by the three groups of w Pip (I, IV, and V) are present as was already shown in Tunisia (Atyame et al ). To verify this hypothesis, we will perform sampling around the Marrakech area.…”

Variation in Wolbachia cidB gene, but not cidA, is associated with cytoplasmic incompatibility mod phenotype diversity in Culex pipiens

“…The screening of the 67 isofemale lines obtained from our sampling in Italy revealed the coexistence of the two mod phenotypes in these Italian populations. However, unlike North African populations in which 8.4% of the isofemale lines were found incompatible when males from these lines were crossed with w PipI‐infected females from the Tunis line (Atyame et al, ; Bonneau, Atyame, et al, ), 92.5% of the isofemale lines from North Italian populations were found incompatible.…”

“…However, the same requirement for the production of live transgenic D. melanogaster and S. cerevisiae could suggest that CidA w Pip protein may simply serve as an antidote (i.e., resc ) to CidB w Pip protein without being directly involved in the mod function (Figure ; Beckmann et al, , ). As we could not conduct a functional transgenic study of the role of cidA wPip in C. pipiens , due to technical restrictions and the amplifications of this gene in the Wolbachia harboured by this species, we investigated here the putative link between CI mod phenotype diversity and variation in its cidA wPip repertoire by sampling new natural populations in North Italy infected with w PipIV Wolbachia , a w Pip phylogenetic group for which simple mod phenotype variations were already screened in North Africa (Atyame et al, ; Bonneau, Atyame, et al, ). The screening of the 67 isofemale lines obtained from our sampling in Italy revealed the coexistence of the two mod phenotypes in these Italian populations.…”

“…As such crosses only differ from each other because of the w Pip strain harboured by the males, the difference in compatibility (i.e., egg‐raft hatching vs. no egg‐raft hatching) between these crosses allows us to qualify the mod phenotype. This way, we demonstrated that mosquitoes infected with w PipIV present two different mod phenotypes: the incompatible mod phenotype, in which males cannot produce viable progenies with females infected with w Pip from group I, II or III, and the compatible mod phenotype, in which males produce viable progenies with such females (Atyame et al, , ; Bonneau, Atyame, et al, ). The association of a specific cidB w Pip variant (variant cidB _IV[a/2]) with the incompatible mod phenotype in 180 isofemale lines (Figure ), together with the results of functional studies in D. melanogaster (Beckmann et al, ; LePage et al, ), demonstrated the involvement of cidB w Pip in mod function and in the diversity of the CI mod phenotype in C. pipiens (Bonneau, Atyame, et al, ).…”