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Facilitating Wolbachia introductions into mosquito populations through insecticide-resistance selection

Facilitating Wolbachia introductions into mosquito populations through insecticide-resistance selection

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Published by Caffy Web
Wolbachia infections are being introduced into mosquito vectors of human dis- Q1
eases following the discovery that they can block transmission of disease
agents. This requires mosquitoes infected with the disease-blockingWolbachia
to successfully invade populations lacking the infection. While this process is
facilitated by features of Wolbachia, particularly their ability to cause cytoplasmic
incompatibility, blocking Wolbachia may produce deleterious effects,
such as reduced host viability or fecundity, that inhibit successful local introductions
and subsequent spatial spread. Here, we outline an approach
to facilitate the introduction and spread of Wolbachia infections by coupling
Wolbachia introduction to resistance to specific classes of insecticides. The
approach takes advantage of very high maternal transmission fidelity of
Wolbachia infections in mosquitoes, complete incompatibility between infected
males and uninfected females, the widespread occurrence of insecticide resistance,
and the widespread use of chemical control in disease-endemic
countries. This approach is easily integrated into many existing control strategies,
provides population suppression during release and might be used to
introduceWolbachia infections even with high and seasonally dependent deleterious
effects, such as the wMelPop infection introduced into Aedes aegypti for
dengue control. However, possible benefits will need to be weighed against
concerns associated with the introduction of resistance alleles.
Wolbachia infections are being introduced into mosquito vectors of human dis- Q1
eases following the discovery that they can block transmission of disease
agents. This requires mosquitoes infected with the disease-blockingWolbachia
to successfully invade populations lacking the infection. While this process is
facilitated by features of Wolbachia, particularly their ability to cause cytoplasmic
incompatibility, blocking Wolbachia may produce deleterious effects,
such as reduced host viability or fecundity, that inhibit successful local introductions
and subsequent spatial spread. Here, we outline an approach
to facilitate the introduction and spread of Wolbachia infections by coupling
Wolbachia introduction to resistance to specific classes of insecticides. The
approach takes advantage of very high maternal transmission fidelity of
Wolbachia infections in mosquitoes, complete incompatibility between infected
males and uninfected females, the widespread occurrence of insecticide resistance,
and the widespread use of chemical control in disease-endemic
countries. This approach is easily integrated into many existing control strategies,
provides population suppression during release and might be used to
introduceWolbachia infections even with high and seasonally dependent deleterious
effects, such as the wMelPop infection introduced into Aedes aegypti for
dengue control. However, possible benefits will need to be weighed against
concerns associated with the introduction of resistance alleles.

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Author Queries
 Journal:
Proceedings of the Royal Society B
 Manuscript:
rspb20130371
Q1
As per journal style, we have italicized the genus name
Wolbachia
throughout the file. Please check.
Q2
Please provide author name and year for unpublished data.
Q3
Please provide expansion for the abbreviation CI.
SQ1
Please confirm that this paper is intended to be Open Access? (The charge for publishing a paper as OpenAccess is £1400 ($2380). Details of the RS policy and charges can be found at http://royalsocietypublishing.org/site/authors/open_access.xhtml. Please note that Open Access publishing is arequirement of certain funding bodies.)
 
rspb.royalsocietypublishing.org
Research
Cite this article:
Hoffmann AA, Turelli M.2013 Facilitating
Wolbachia
introductionsinto mosquito populations through insecticide-resistance selection. Proc R Soc B 20130371.http://dx.doi.org/10.1098/rspb.2013.0371Received: 13 February 2013Accepted: 18 March 2013
Subject Areas:
genetics, evolution, health and disease andepidemiology
Keywords:
symbiont, pesticide, disease vector, invasion,resistance
Author for correspondence:
Ary A. Hoffmanne-mail:ary@unimelb.edu.au
Facilitating
Wolbachia
introductionsinto mosquito populations throughinsecticide-resistance selection
Ary A. Hoffmann
1
and Michael Turelli
2
1
Departments of Genetics and Zoology, Bio21 Institute, The University of Melbourne, Parkville,Victoria 3010, Australia
2
Department of Evolution and Ecology, University of California, Davis, CA 95616, USA
Wolbachia
Q1
infections are beingintroducedinto mosquitovectors of humandis-eases following the discovery that they can block transmission of diseaseagents. This requires mosquitoes infected with the disease-blocking
Wolbachia
to successfully invade populations lacking the infection. While this process isfacilitated by features of 
Wolbachia
, particularly their ability to cause cyto-plasmic incompatibility, blocking
Wolbachia
may produce deleterious effects,such as reduced host viability or fecundity, that inhibit successful local intro-ductions and subsequent spatial spread. Here, we outline an approachto facilitate the introduction and spread of 
Wolbachia
infections by coupling
Wolbachia
introduction to resistance to specific classes of insecticides. Theapproach takes advantage of very high maternal transmission fidelity of 
Wolbachia
infectionsinmosquitoes,completeincompatibilitybetweeninfectedmalesand uninfectedfemales,thewidespreadoccurrenceofinsecticide resist-ance, and the widespread use of chemical control in disease-endemiccountries. This approach is easily integrated into many existing control strat-egies, provides population suppression during release and might be used tointroduce
Wolbachia
infections even with high and seasonally dependent dele-terious effects,suchasthe
w
MelPopinfectionintroducedinto
Aedes aegypti
fordengue control. However, possible benefits will need to be weighed againstconcerns associated with the introduction of resistance alleles.
1. Introduction
There is increasing interest in using
Wolbachia
bacterial infections to suppressmosquito-transmitted diseases. This follows the successful introduction of 
Wolbachia
into disease vectors, particularly
Aedes aegypti
Linnaeus, 1762 [1]and
Aedes albopictus
Skuse, 1894 [2], and the realization that
Wolbachia
act asnatural agents to suppress disease [3,4]. Several experiments have shown that
Wolbachia
can suppress dengue, chikungunya, yellow fever and other diseases[5], and that they might even be effective against other diseases includingmalaria [6]. Maternally inherited
Wolbachia
possess several characteristics thatfacilitate their invasion and rapid spread into natural populations [7], particu-larly their ability to cause cytoplasmic incompatibility that leads to embryodeath when uninfected females mate with infected males.Preliminary field trials on
A. aegypti
infected with the
w
Mel
Wolbachia
havedemonstrated successful invasion of two sites in northern Australia [8]. Thisinfection appears stable and is present at a frequency approaching 100 percent at these sites more than a yearafter the invasion was initiated
Q2
(unpublisheddata). However, this infection has relatively minor deleterious effects [1],facilitating its establishment because there is a relatively low unstable equili- brium point that has to be exceeded for invasion. Other
Wolbachia
strainswith the potential to provide stronger blockage of disease transmission mayhave much larger deleterious effects, making initial invasion and particularlysubsequent spatial spread difficult or impossible [9]. In particular, the
w
MelPop
&
2013 The Authors. Published by the Royal Society under the terms of the Creative Commons AttributionLicense http://creativecommons.org/licenses/by/3.0/, which permits unrestricted use, provided the originalauthor and source are credited.
123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960616263
ARTICLE IN PRESS
rspb20130371—26/3/13—17:57–Copy Edited by: Uma C
 
infection provides complete blockage of dengue [5], but
 A. aegypti
mosquitoes with this infection suffer significantlyreduced fecundity and egg hatch, particularly when eggsare in a dry quiescent state [10,11]. This feature makes it more difficult to introduce
w
MelPop into populations asreflected by its rate of increase in semi-natural populationcages when compared with
w
Mel [1]. Moreover, successfulinvasion of 
w
MelPop into natural populations is likely torequire releasing many infected mosquitoes to overcomethe higher unstable equilibrium point [10]. Whereas
w
Melsuccessfully invaded populations over three months whenreleases increased natural adult populations by 1.5–2 times[8], local invasions by infections such as
w
MelPop over asimilar time scale are likely to require introduction rates lead-ing to a transient increase in adult population size of greaterthan twofold. The resultant increase in mosquito biting ratemay become unacceptable to local community membersparticularly in disease-endemic areas. Once introduced intoa local area, the infection may be lost following mosquitomigration from surrounding uninfected populations [9] orduring the dry season when
w
MelPop imposes a substantialfitness cost [10].To counter theseissues,a method isneededtofacilitate thespread of 
Wolbachia
that is consistent with current controlmethods and acceptable in countries where diseases are ende-mic. One possibility is to integrate
Wolbachia
releases withpesticide applications by introducing insecticide resistanceinto the
Wolbachia
-infected line. Resistance is widespread inmosquitoes including disease vectors such as
A. aegypti
, andresistance evolution has led to chemical methods of control becoming ineffective and being abandoned in some instances[12,13]. At first sight, this strategy might seem doomed to failure because any association between the nuclear-basedresistance alleles and the maternally inherited
Wolbachia
inthe released strain is expected to break down rapidly after
Wolbachia
are introduced [14]. However, as we argue below,there are unique features of mosquito–
Wolbachia
infectionsthat make this strategy attractive, providing a potential pathfor introducing
Wolbachia
into local populations more easilyand without increasing mosquito populations. The strategycould also help secure the persistence of infections such as
w
MelPop across a dry season and assist their spatial spread,as long asthe unstable equilibrium (the frequencyof 
Wolbachia
in a population that needs to be exceeded for the
Wolbachia
tospread to fixation) is not prohibitively high [9].
2. Approach
We assume that resistance can be selected in a mosquitopopulation infected by
Wolbachia
. In
A. aegypti
, there is no evi-dence that
Wolbachia
infections directly influence resistanceto commonly used chemicals [15]. By contrast, selection onthe nuclear genome of mosquitoes can readily increase resist-ance to a range of pesticides including organophosphates,pyrethroids and organochlorines [12,16]. Resistant
Wolbachia
-infected populations might be established through a varietyof means. Resistance could be identified in field populations,and then introduced into infected strains by backcrossing tothe field populations, particularly when combined withongoing screening for resistance, in the same way as
Wolbachia
strainshavebeenbackcrossedtointroducethebackgroundofatarget natural population prior to release [10]. Selection forresistance could also take place within the background of aninfected population by applying a laboratory-based methodfor increasing resistance [16]. Finally a resistant populationcould be developed independently in the laboratory throughselection ormutagenesis,and
Wolbachia
could be subsequentlyintroduced into this population through backcrossing. Withthese approaches, it should be possible to establish infectedpopulations resistant to different chemicals on various gene-tic backgrounds, with the resistant phenotype maintainedthrough regular exposure to discriminatory doses.Potential targets for resistance screening are the chemicalswidely applied for mosquito control, such as organopho-sphates applied to larval breeding sites, or pyrethroid andorganophosphate adulticides used in fogging buildings andsurrounding areas [17]. Resistance to these chemicals has been detected in some
Aedes
mosquito populations [12,13], making it feasible to select for resistance or identify naturalpopulations with resistance. It should also be possible todevelop resistance to chemicals or formulations that are notused for routine mosquito control, a strategy that might beacceptable to the community and to regulatory authorities.Once infected populations resistant to chemicals have been developed, they can be introduced into natural popula-tions through releases. Any disequilibrium between
Wolbachia
and its nuclear background is expected to be roughly halvedeach generation when the infection is being introduced[18]. Under imperfect maternal transmission of the
Wolbachia
infection and incomplete cytoplasmic incompatibility—the situation for the
w
Ri infection of 
Drosophila simulans
(Sturtevant), which has been extensively characterized[19]—uninfected individuals will arise with the nuclear background of the infected population and vice versa. How-ever, in naturally infected populations of 
Culex
and
Aedes
mosquitoes, the failure rate of maternal transmission,
, is 0or very near 0, and cytoplasmic incompatibility is completeor very nearly complete [20,21]. This means that whereas matings between infected males and uninfected females donot produce any offspring, the progeny of infected femalesare always viable and infected. Moreover, in lines of artifi-cially infected
Aedes
mosquitoes, it also appears that
¼
0and there is complete or near-complete incompatibility[1,10]. Thus, in these infections the association between
Wolbachia
infection and nuclear-resistance alleles is expectedto break down only in one direction, with infected individ-uals acquiring susceptibility alleles through mating withuninfected males, but no transfer of resistance alleles fromthe release stock to the
Wolbachia
-uninfected component of the mosquito population.The potential impact of resistance on
Wolbachia
invasionscan be illustrated by considering two aspects of 
Wolbachia
releases, the position of the unstable point for invasion andthe speed at which invasion can take place.To explore potential effects of coupling resistance alleles to
Wolbachia
introductions on unstable points, we present ideal-ized analyses aimed at approximating the quantitative effectsrather than capturing specific biological details. To simplifythealgebra,we assume discretegenerationsandthat
Wolbachia
affects female fecundity, with infected females having relativefecundity
F
¼
1
2
s
, with
s
.
0. As noted below, the par-ameter
F
can also approximate viability effects attributableto
Wolbachia
. We assume perfect maternal
Wolbachia
trans-mission and complete CI
Q3
(as seen for the
w
MelPop and
w
Melinfections—[1,10,11]) and for simplicity we also assume
r     s      p   b     .r     o     y   a  l        s    o   c   i        e   t        y     p   u   b    l       i        s   h    i       n     g   . o  r       g  P    r     o   c   R     S      o   c    B    2     0    1     3     0     3    7    1    
2
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ARTICLE IN PRESS
rspb20130371—26/3/13—17:57–Copy Edited by: Uma C

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