Abstract
The development of sex-specific traits, including the female-specific ability to bite humans and vector disease, is critical for vector mosquito reproduction and pathogen transmission. Doublesex (Dsx), a terminal transcription factor in the sex determination pathway, is known to regulate sex-specific gene expression during development of the dengue fever vector mosquito Aedes aegypti. Here, the effects of developmental siRNA-mediated dsx silencing were assessed in adult females. Targeting of dsx during A. aegypti development resulted in decreased female wing size, a correlate for body size, which is typically larger in females. siRNA-mediated targeting of dsx also resulted in decreased length of the adult female proboscis. Although dsx silencing did not impact female membrane blood feeding or mating behavior in the laboratory, decreased fecundity and fertility correlated with decreased ovary length, ovariole length, and ovariole number in dsx knockdown females. Dsx silencing also resulted in disruption of olfactory system development, as evidenced by reduced length of the female antenna and maxillary palp and the sensilla present on these structures, as well as disrupted odorant receptor expression. Female lifespan, a critical component of the ability of A. aegypti to transmit pathogens, was also significantly reduced in adult females following developmental targeting of dsx. The results of this investigation demonstrate that silencing of dsx during A. aegypti development disrupts multiple sex-specific morphological, physiological, and behavioral traits of adult females, a number of which are directly or indirectly linked to mosquito reproduction and pathogen transmission. Moreover, the olfactory phenotypes observed connect Dsx to development of the olfactory system, suggesting that A. aegypti will be an excellent system in which to further assess the developmental genetics of sex-specific chemosensation.
Highlights
Most animal species display sexually dimorphic behaviors, the majority of which are linked to sexual reproduction [1]
For analysis of structures/traits that develop in the late pupal stage, dsx-KD A or dsx-KD B small interfering RNA (siRNA) was delivered through pupal microinjection, which generates more effective silencing at the late pupal stage, at which time some recovery of dsx expression is observed in animals that were fed chitosan/siRNA nanoparticles as larvae (S1 Fig)
Female mosquitoes differ from males in several morphological, physiological, and behavioral traits that are critical to their ability to transmit diseases
Summary
Most animal species display sexually dimorphic behaviors, the majority of which are linked to sexual reproduction [1]. Disease vector mosquitoes are excellent subjects for studies that explore the biological basis of sexual dimorphism. Adult female mosquitoes, which require blood meals for reproduction, bite humans and transmit pathogens. Females differ from males in morphological, physiological, and behavioral traits that are critical components of their ability to spread diseases, including feeding behaviors, longevity, and susceptibility to infections. Researchers have had a long-standing interest in the potential to manipulate genetic components of the sex determination pathway and sexual differentiation for vector control. The genes that regulate sex-specification and development of mosquito sexual dimorphism may represent novel targets for vector control, most of these genes have not yet been functionally characterized in vector mosquitoes
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