Stable coexistence of incompatible Wolbachia along a
narrow contact zone in mosquito field populations
CE
´
LESTINE M. ATYAME,* †‡ PIERRICK LABBE
´
,* ‡ FRANC ß OIS ROUSSET,* ‡ MARWA BEJI, §
PATRICK MAKOUNDOU,* ‡ OLIVIER DURON,* ‡
1
EMILIE DUMAS,* ‡ NICOLE PASTEUR,* ‡
ALI BOUATTOUR, § PHILIPPE FORT ‡ ¶ and MYLE
`
NE WEILL* ‡
*CNRS, ISEM—UMR 5554, Montpellier, France, †University La Re ´union/CRVOI, Ste Clotilde, Re ´union Island, France,
‡University Montpellier 2, Montpellier, France, §Institut Pasteur Tunis, Laboratory of Epidemiology and Veterinary
Microbiology/University Tunis El Manar, Tunis, Tunisia, ¶CNRS, CRBM—UMR 5237, Montpellier, France
Abstract
In arthropods, the intracellular bacteria Wolbachia often induce cytoplasmic incompati-
bility (CI) between sperm and egg, which causes conditional embryonic death and pro-
motes 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 sepa-
rating their distribution areas. Crossing experiments with isofemale lines from differ-
ent 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 dis-
persal 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.
Keywords: contact zone, Culex pipiens mosquito, cytoplasmic incompatibility, Wolbachia
Received 28 July 2014; revision received 2 December 2014; accepted 3 December 2014
Introduction
Wolbachia are maternally inherited intracellular a-prote-
obacteria that infect many arthropod species (Werren
et al. 2008). Wolbachia are the most frequent bacterial
endosymbiont described so far in insects, infecting
20–70% of species (Werren et al. 1995; Jeyaprakash &
Hoy 2000; Hilgenboecker et al. 2008; Zug & Hammer-
stein 2012). This evolutionary success is mainly attrib-
uted to the ability of Wolbachia to manipulate the host
reproductive system to its own advantage (Werren et al.
2008). The most common manipulation is cytoplasmic
incompatibility (CI), which triggers embryonic mortality
when infected males mate with uninfected females,
whereas the reciprocal cross remains compatible. Thus,
infected females have a reproductive advantage in
polymorphic populations which allows the spread of
Correspondence: Ce ´lestine M. Atyame, Fax: (262) 262 93 88 01;
E-mail: celestine.atyame-nten@univ-reunion.fr
1
Current address: MIVEGEC—UMR 5290-224, CNRS-IRD-
UM1-UM2, Montpellier, France
© 2014 John Wiley & Sons Ltd
Molecular Ecology (2014) doi: 10.1111/mec.13035