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A Wolbachia Symbiont in Aedes Aegypti Disrupts Mosquito Egg Development to a Greater Extent When Mosquitoes Feed on Nonhuman Versus Human Blood

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A Wolbachia Symbiont in Aedes Aegypti Disrupts Mosquito Egg Development to a Greater Extent When Mosquitoes Feed on Nonhuman Versus Human Blood ARTHROPOD/HOST INTERACTION,IMMUNITY A Wolbachia Symbiont in Aedes aegypti Disrupts Mosquito Egg Development to a Greater Extent When Mosquitoes Feed on Nonhuman Versus Human Blood 1,2 1,3 1,4 CONOR J. MCMENIMAN, GRANT L. HUGHES, AND SCOTT L. O’NEILL J. Med. Entomol. 48(1): 76Ð84 (2011); DOI: 10.1603/ME09188 ABSTRACT A vertebrate bloodmeal is required by female mosquitoes of most species to obtain nutrients for egg maturation. The yellowfever mosquito, Aedes aegypti (L.), feeds predominantly on humans, despite having the capacity to use blood from other hosts for this process. Here, we report that female Ae. aegypti infected with a virulent strain of the intracellular bacterium Wolbachia pipientis (wMelPop) from Drosophila melanogaster (Meigen) have a reduced ability to use blood for egg development. Blood feeding by wMelPop-infected females on mouse, guinea pig, or chicken hosts resulted in a near complete abolishment of reproductive output associated with both a decline in the numbers of eggs oviposited as well as the hatching rate of successfully laid eggs. In contrast, the reproductive output of wMelPop-infected females fed human blood was only mildly affected in comparison to individuals fed animal blood sources. Blood-feeding assays over two reproductive cycles deÞnitively illustrated a nutritional interaction between host blood source and egg development in wMelPop-infected Ae. aegypti. Removal of Wolbachia from mosquitoes using antibiotic treatment rescued egg development on all blood sources. Further investigation of this phenotype may provide new insights into the nutritional basis of mosquito anthropophily. KEY WORDS Wolbachia, reproduction, mosquito, anthropophily Female mosquitoes of most species must ingest a ver- fecundity of Ae. aegypti, compared with other verte- tebrate bloodmeal to obtain nutrients required for egg brate hosts (Scott et al. 1997, Costero et al. 1998, development (Attardo et al. 2005). The preference for Harrington et al. 2001, Braks et al. 2006). A greater human blood by a number of mosquito species (an- understanding of the nutritional basis of anthropoph- thropophily) aids in the transmission of human patho- ily may provide insight into important factors associ- gens such as dengue and malaria (Besansky et al. ated with host preference for humans, and potentially 2004). Aedes aegypti (L.), the principal vector of den- assist in the rational design of strategies that interfere gue, is a highly anthropophilic mosquito that lives in with this behavior. and around human habitation. Previous studies have A novel method for the control of dengue that has determined that Ae. aegypti feeds predominantly on been proposed involves the introduction of strains of humans in the Þeld (Scott et al. 1993b, Ponlawat and the obligate intracellular bacterium Wolbachia pipi- Harrington 2005), often taking bloodmeals multiple entis into Ae. aegypti populations to modify mosquito times within a single gonotrophic cycle (Scott et al. population age structure (Sinkins and OÕNeill 2000, 1993a, 2000). Cook et al. 2008) as well as directly modulate vector The nutritional components of human blood that competence (Moreira et al. 2009). Wolbachia are ma- differentiate it from other blood sources and subse- ternally transmitted endosymbionts that naturally in- quently contribute to the preference of Ae. aegypti for fect a wide diversity of invertebrates (Hilgenboecker humans are not fully understood (Harrington et al. et al. 2008), including many medically important mos- 2001). Blood feeding on humans has been shown to quito species (Sinkins 2004). Previously, we described increase energy reserves, survival rate, and lifetime the stable introduction of a virulent Wolbachia strain (wMelPop) from Drosophila melanogaster (Meigen) into Ae. aegypti (McMeniman et al. 2009), a species not 1 School of Biological Sciences, The University of Queensland, QLD naturally infected with Wolbachia. 4072, Australia. 2 Current address: Laboratory of Neurogenetics and Behavior, The One major physiological difference between D. Rockefeller University, 1230 York Ave., New York, NY 10065. melanogaster and Ae. aegypti is the requirement for the 3 Current address: The W. Harry Feinstone Department of Molec- latter species to blood feed to obtain nutrients for ular Microbiology and Immunology, Bloomberg School of Public oogenesis. In Drosophila, Wolbachia bacteria are Health and Malaria Research Institute, Johns Hopkins University, 615 North Wolfe St., Baltimore, MD 21205. thought to be dependent on their hosts for a range of 4 Corresponding author, e-mail: [email protected]. metabolites including amino acids, iron, and lipids 0022-2585/11/0076Ð0084$04.00/0 ᭧ 2011 Entomological Society of America January 2011 MCMENIMAN ET AL.: Wolbachia AND Ae. aegypti EGG DEVELOPMENT 77 (Wu et al. 2004, Brownlie and OÕNeill 2006, Brownlie Research, Animal Ethics Protocol P361). Written con- et al. 2009), which are also essential for mosquito egg sent was obtained from all human subjects used for development (Ziegler and Ibrahim 2001, Attardo et al. blood feeding. 2006, Zhou et al. 2007). Despite this potential conßict, To assess the ability of wMelPop-infected Ae. ae- wMelPop-infected Ae. aegypti are able to use blood gypti to use the blood from a wider range of host from humans, their preferred host, for egg develop- species for egg development, we conducted standard- ment with minimal costs to reproductive Þtness for ized membrane-feeding trials. For membrane feeding, young females (McMeniman et al. 2009). fresh whole mouse, chicken, and sheep blood antico- In this study, we examined the effect of wMelPop agulated with trisodium citrate (4 mg/ml), and deÞ- infection on the ability of this mosquito to use less brinated sheep blood, were purchased from a com- preferred nonhuman blood sources for egg develop- mercial supplier (IMVS Veterinary Services Division, ment. Here, we report that female Ae. aegypti infected Gilles Plains, SA, Australia). Anticoagulated (4 mg/ml with wMelPop have a drastically reduced ability to use trisodium citrate) and deÞbrinated pig blood were blood from nonhuman hosts for this process. We used sourced from a local abattoir (KR Castlemaine, blood from a wide variety of animal hosts, and anti- Toowoomba, QLD, Austrailia). Bloodmeals were pre- biotic clearance of Wolbachia to demonstrate an in- sented to premated 5-d-old females in glass membrane teraction between blood source and wMelPop infec- feeders (Rutledge et al. 1964) maintained at 37ЊC and tion that profoundly inßuences egg development in Þtted with Hemotek collagen membrane (Discovery Ae. aegypti. Workshops, Accrington, Lancashire, United King- dom). All bloodmeals were supplemented with 1 mM ATP to stimulate engorgement (Kogan 1990). Imme- Materials and Methods diately after a set feeding period of 30 min, unfed Mosquito Strains and Rearing. The following Ae. females were removed from treatment cages. aegypti strains were used in this study: 1) the In both laboratory animal and membrane feeding wMelPop-infected strains PGYP1 and PGYP2; 2) trials, sucrose sources were removed from females 5 h their uninfected tetracycline-cured counterparts before blood feeding. Postfeeding, blood-fed females PGYP1.tet and PGYP2.tet; and 3) the uninfected wild- were provided with constant access to 10% sucrose type strain JCU, from which PGYP1 and PGYP2 were solution and water until fecundity and fertility assays originally derived upon transinfection with wMelPop were done. (McMeniman et al. 2009). Mosquitoes were main- Blood-Feeding Trials: Human Volunteers. To ex- tained at 25ЊC, 75Ð85% RH, and a photoperiod of 12:12 amine variation in fecundity associated with blood (L:D) h. Larvae were reared at set density (150 larvae sources from different individual humans, PGYP1 and per 3 liters of distilled water in 30- by 40- by 8-cm PGYP1.tet mosquitoes were fed on eight human vol- plastic trays) and fed 150 mg of Þsh food (TetraMin unteers (four male and four female) in four replicate Tropical Tablets, Tetra, Melle, Germany) per pan experiments. Sucrose sources were removed5hbe- each day until pupation. Adults were kept in screened fore blood feeding and premated 5-d-old adult females 30- by 30- by 30-cm cages with ad libitum access to 10% mosquitoes were allowed to feed on exposed forearms sucrose solution and water. Five day old females were for twenty minutes (University of Queensland, Hu- provided with a human bloodmeal (University of man Ethics Approval 2007001379). In each of the four Queensland, Human Ethics Approval 2007001379) for replicates, the left and right arms were alternated for egg production. For routine colony maintenance, eggs the wMelPop-infected PGYP1 and tetracycline- from the PGYP1 and PGYP2 strains were hatched 5Ð7 treated PGYP1.tet mosquitoes. Postblood feeding, the d postoviposition (i.e., without prolonged desicca- sucrose source was returned. tion) to initiate the next generation. Fecundity and Egg Viability Assays. Females were Tetracycline Treatment. The tetracycline-cured isolated individually for egg-laying 96 h postblood PGYP1.tet and PGYP2.tet strains of Ae. aegypti were meal for a period of 48 h in plastic Drosophila vials generated at G8 and G11 posttransinfection by the containing wet Þlter paper as an oviposition substrate. addition of tetracycline (1 mg/ml) to the adult diet and Eggs were hatched 120 h after oviposition by submer- recolonized with resident gut microßora from wild-type sion in nutrient-infused deoxygenated water (75 mg larvae
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