Wolbachia pipientisassociated to tephritid fruit fly pests: from basic research to applications

Abstract

23hominivorax Coquerel); several species of tsetse fly (Glossina spp.); and the codling 71 moth (Cydia pomonella L.) [reviewed in 17, 18]. 72 73 Successful SIT programs as part of Area-wide Integrated Pest Management (IPM) 74 strategies have also been implemented for several tephritids: Ceratitis capitata 75 Wiedemann; Anastrepha ludens Loew; Anastrepha obliqua Macquart; Anastrepha 76 fraterculus Wiedemann; Zeugodacus cucurbitae Coquillett; Bactrocera dorsalis Hendel; 77and Bactrocera tryoni Froggatt [6, 12, 13, 15]. SIT is currently being developed for two 78 additional tephritid species: Dacus ciliatus Loew and Bactrocera tau Walker [19, 20]. 79The advantages of the SIT over other pest control approaches (e.g. use of pesticides) 80 are that it is the most environmentally friendly and resistance is unlikely to evolve [21, 81 22]. 82 83 Another autocidal strategy where mating between mass-reared and wild insects can be 84 used to suppress pest populations is the incompatible insect technique (IIT). IIT also 85 relies on the principle of reducing female fertility, but utilizes endosymbiotic bacteria 86 instead of radiation, to induce a context-dependent sterility in wild females. It is based 87 on the ability of certain maternally inherited bacteria (namely from the genus Wolbachia) 88to induce a form of reproductive incompatibility known as cytoplasmic incompatibility (CI; 89 explained in the section below). Herein we review the current knowledge on taxonomic 90 diversity of Wolbachia-tephritid associations and their phenotypic consequences, and 91 identify gaps in knowledge and approaches in the context of potential application of IIT in 92 AW-IPM programs to control tephritid pests. We also discuss scenarios where these 93 two autocidal strategies, SIT and IIT, could be potentially combined for the population 94 suppression of tephritid pests. 95 96 5 The influence of Wolbachia on host ecology 97Insects and other arthropods are common hosts of maternally inherited bacteria 98 [reviewed in 23]. These heritable endosymbionts can have a strong influence on host 99 ecology. Such vertically transmitted bacteria are typically vastly (or fully) dependent on 100 the host for survival and transmission. Certain associations are obligate for both 101 partners, and generally involve a nutritional benefit to the host. Other heritable bacteria 102 are facultative, with such associations ranging from mutualistic to parasitic from the 103 host's perspective. Among these, Wolbachia is the most common and widespread 104 facultative symbiont of insects and arthropods [24][25][26][27]. 105 106 Wolbachia is a diverse and old genus [possibly older than 200 million years; 28] of 107 intracellular gram-negative Alphaproteobacteria (within the order Rickettsiales) 108 associated with arthropods and filarial nematodes. Wolbachia cells resemble small 109 spheres 0.2-1.5 μ m, occur in all tissue types, but tend to be more prevalent in ovaries 110 and testicles of infected hosts, and are closely associated with the female germline 111 [...

Effect of host fruit, temperature and Wolbachia infection on survival and development of Ceratitis capitata immature stages

“…In general, the significant role of microbiota (Wolbachia, gut bacteria etc.) in tephritid biology and behavior is widely accepted [65,104]. However, the interaction among the different bacterial communities and the way that these interactions affect insect's biology and behavior are not completely unraveled.…”

“…The following general patterns emerged: a) Wolbachia causes high egg-to-larva mortality, b) Wolbachia causes high egg-to-adult mortality (exception: Vienna 8 GSS + wCer2) and c) Wolbachia shortens egg-to-adult developmental time, although it prolongs embryonic development (exception: Benakeio + wCer2). Recent studies by Kyritsis [65,66] on the same system (Wolbachia-medfly) reported no effects of Wolbachia infection on adult lifespan and a reduced fecundity in the case of wCer4 infection only. Even though wCer2 and wCer4 in general tended to have consistent effects on medfly, the magnitude of their effects differed.…”

Old residents and new arrivals ofRhagoletisspecies in Europe

“…Recently, much interest has been shown on studies regarding the intracellular bacterium Wolbachia that is found in more than 40% of the terrestrial arthropod species (Werren et al , 2008; Zug & Hammerstein, 2012). The presence of Wolbachia has been associated with the induction of a variety of host reproductive phenotypes such as feminization, parthenogenesis, male killing and cytoplasmic incompatibility (CI) (for review see Werren et al , 2008; Saridaki & Bourtzis, 2010; Mateos et al , 2019). For these reasons, Wolbachia is considered a key player affecting biological and evolutionary processes as well as a tool for the control of agricultural pests and disease vectors (Werren et al , 2008; Saridaki & Bourtzis, 2010; Mateos et al , 2019).…”

“…Augustinos and colleagues (2014) pointed to the presence of additional uncharacterized Wolbachia strains on R. cerasi populations from Greece, and raised concerns about the suitability of the currently used diagnostic markers for genotyping. Considering the information mentioned earlier, along with the fact that Wolbachia cannot be cultivated in the laboratory, the presence of low-titre infections and/or multiple infections in the same individual, as well as the highly recombinant nature of the bacterial chromosome, make Wolbachia characterization in R. cerasi samples a very difficult task (Zabalou et al , 2004, 2009; Schneider et al , 2013; Mateos et al , 2019). Allelic intersection analysis provided an additional tool for the characterization of multiple Wolbachia infections in R. cerasi (Arthofer et al , 2011); however, this analysis requires a priori knowledge on the Wolbachia strains harboured by a species and can be quite laborious.…”

Transinfection of buffalo flies (Haematobia irritans exigua) with Wolbachia and effect on host biology

“…Wolbachia are maternally inherited endosymbionts of insects, that are of much interest for use in the biological control of pests, most particularly as a basis for area-wide integrated control strategies for a range of insect species [9][10][11]. Wolbachia has been used in insect control programmes in two main ways.…”