Identity and transfer of male reproductive gland proteins of the dengue vector mosquito, Aedes aegypti: Potential tools for control of female feeding and reproduction

Abstract

Male reproductive gland proteins (mRGPs) impact the physiology and/or behavior of mated females in a broad range of organisms. We sought to identify mRGPs of the yellow fever mosquito, Aedes aegypti, the primary vector of dengue and yellow fever viruses. Earlier studies with Ae. aegypti demonstrated that "matrone" (a partially purified male reproductive accessory gland substance) or male accessory gland fluid injected into virgin female Ae. aegypti affect female sexual refractoriness, blood feeding and digestion, flight, ovarian development, and oviposition. Using bioinformatic comparisons to Drosophila melanogaster accessory gland proteins and mass spectrometry of proteins from Ae. aegypti male accessory glands and ejaculatory ducts (AG/ED) and female reproductive tracts, we identified 63 new putative Ae. aegypti mRGPs. Twenty-one of these proteins were found in the reproductive tract of mated females, but not of virgin females, suggesting that they are transferred from males to females during mating. Most of the putative mRGPs fall into the same protein classes as mRGPs in other organisms, although some appear to be evolving rapidly and lack identifiable homologs in Culex pipiens, Anopheles gambiae, and D. melanogaster. Our results identify candidate male-derived molecules that may have an important influence on behavior, survival and reproduction of female mosquitoes.

Morphological and morphometrical assessment of spermathecae of Aedes aegypti females

“…In addition to affecting female behaviour, the spermathecal fluid also participates on the maturation of the spermatozoa after mating (Giuffrida et al 1995). Besides spermatozoa, mosquito spermathecae also store proteins from male seminal fluid (Sirot et al 2008, Thailayil et al 2011. We speculate that in spite of the presence of a relatively thick spermathecal cuticle (0.7 µm) (Clements & Potter 1967) male proteins might be capable of reaching the haemolymph.…”

Anopheles gambiaemales produce and transfer the vitellogenic steroid hormone 20-hydroxyecdysone to females during mating

“…In A. aegypti, a MAG effect is mediated by the matrone peptide, which may stimulate vitellogenesis (9). Many Acps, which have been recently identified in Aedes males and mated females, are also suspected to influence female after mating (43). Additionally, JH, which is involved in ovarian follicle development to the pre-vitellogenic resting stage in female mosquitoes, is synthesized and stored in Aedes MAGs and possibly transferred to the female during mating (44).…”

Proteomics enhances evolutionary and functional analysis of reproductive proteins

“…A recent explosion of proteomics studies has identified many reproductive proteins in taxa ranging from crickets and honeybees to rodents and humans. (15,(26)(27)(28)(29)(30)(31)(32)(33)(34)(35)(36)(37)(38)(39)(40) Applying mass spectrometry (MS)-based proteomics to the study of reproduction has been particularly fruitful, in our view, because reproductive tissues are often specialized cell types with the discrete function of producing proteins involved in a specific biological process. Thus, biochemical isolation and purification of proteins from these tissues and cell types are straightforward, and large amounts of relatively pure protein mixtures can be analyzed by MS.…”

“…May present odorants, pheromones or other small molecules to receptors in female reproductive tract (32) Leucyl aminopeptidases D. melanogaster sperm Possible involvement in acrosome reaction (31) Iron regulation and blood clotting Aedes aegypti (mosquito) seminal fluid proteins Possible localization to midgut after transfer to female reproductive tract, where proteins could help process blood meals that are necessary for egg production (38) Antioxidant defense enzymes Apis mellifera (honeybee) female spermatheca…”