Whole blood and blood components from vertebrates differentially affect egg formation in three species of anautogenous mosquitoes

Ruby E Harrison,Mark R Brown,Michael R Strand

doi:10.1186/s13071-021-04594-9

Abstract

BackgroundMost female mosquitoes are anautogenous and must blood feed on a vertebrate host to produce eggs. Prior studies show that the number of eggs females lay per clutch correlates with the volume of blood ingested and that protein is the most important macronutrient for egg formation. In contrast, how whole blood, blood fractions and specific blood proteins from different vertebrates affect egg formation is less clear. Since egg formation is best understood in Aedes aegypti, we examined how blood and blood components from different vertebrates affect this species and two others: the malaria vector Anopheles gambiae and arbovirus vector Culex quinquefasciatus.MethodsAdult female mosquitoes were fed blood, blood fractions and purified major blood proteins from different vertebrate hosts. Markers of reproductive response including ovary ecdysteroidogenesis, yolk deposition into oocytes and number of mature eggs produced were measured.ResultsAe. aegypti, An. gambiae and C. quinquefasciatus responded differently to meals of whole blood, plasma or blood cells from human, rat, chicken and turkey hosts. We observed more similarities between the anthropophiles Ae. aegypti and An. gambiae than the ornithophile C. quinquefasciatus. Focusing on Ae. aegypti, the major plasma-derived proteins (serum albumin, fibrinogen and globulins) differentially stimulated egg formation as a function of vertebrate host source. The major blood cell protein, hemoglobin, stimulated yolk deposition when from pigs but not humans, cows or sheep. Serum albumins from different vertebrates also variably affected egg formation. Bovine serum albumin (BSA) stimulated ovary ecdysteroidogenesis, but more weakly induced digestive enzyme activities than whole blood. In contrast, BSA-derived peptides and free amino acids had no stimulatory effects on ecdysteroidogenesis or yolk deposition into oocytes.ConclusionsWhole blood, blood fractions and specific blood proteins supported egg formation in three species of anautogenous mosquitoes but specific responses varied with the vertebrate source of the blood components tested.Graphical

Highlights

Most female mosquitoes are anautogenous and must blood feed on a vertebrate host to produce eggs
ECD released from follicle cells is converted to 20-hydroxyecdysone (20E) in fat body adipocytes, which together with nutrient signaling via the target of rapamycin (TOR) pathway stimulates the synthesis of vitellogenin (Vg) and other yolk components [16]
UGAL strain Aedes aegypti respond to blood feeding on a rat or membrane feeders containing rat blood We first assessed whether females exhibited any differences in feeding, survival, oviposition or number of eggs laid when given an anesthetized rat versus membrane feeders filled with commercially purchased bottled blood

Summary

Introduction

Most female mosquitoes are anautogenous and must blood feed on a vertebrate host to produce eggs. Mosquitoes vector a number of bloodborne pathogens, including the causative agents of malaria, dengue fever and yellow fever, that annually result in > 200 million human infections and 725,000 deaths worldwide [1]. The ability to blood feed and produce eggs in consecutive cycles over a lifespan of 4–8 weeks further underlies how anautogenous mosquitoes acquire and transmit pathogens among vertebrate hosts [4]. The processes regulating the vitellogenic phase are currently best understood in Aedes aegypti where consumption of a bloodmeal stimulates the release of two types of peptide hormones, ovary ecdysteroidogenic hormone (OEH) and insulin-like peptides (ILPs), from the brain [6]. Females lay up to 120 eggs in a single clutch by 72 h post-bloodmeal [4]

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