Maximizing horizontal transmission through mating: increased mating frequency and mating competitiveness associated...

Microsporidia MB is a naturally occurring symbiont in Anopheles arabiensis mosquitoes that inhibits the development of Plasmodium. It is transmitted both vertically and horizontally, enabling its spread within mosquito populations. Currently, mating is the only known mechanism for horizontal transmission. Understanding the factors that influence Microsporidia MB transmission during mating is crucial for developing a malaria transmission-blocking strategy based on this symbiont.

The effect of mosquito age on Microsporidia MB transmission was determined through mating bioassays between infected and uninfected Anopheles arabiensis males and females in three age groups: 3-4 days, 7-8 days, and 10-11 days. Mating bioassays were also conducted to determine if Microsporidia MB infection affects the individual male mating frequencies and mating competitiveness of male mosquitoes. To assess the effect of Microsporidia MB-infection on swarming under field conditions, swarming and non-swarming An. arabiensis male mosquitoes were collected and compared for Microsporidia MB prevalence.

The age of mosquitoes does not affect the transmission of Microsporidia MB from males to females (χ² = 11.6, df = 12, p = 0.47). However, transmission of the Microsporidia MB from female mosquitoes to males was not observed in the 3-4 days old age group. Although heterogeneous, there is higher overall transmission from male to female (41.5%) compared to female to male (22.4%). When individual males (Microsporidia MB infected or uninfected) were mated with females, Microsporidia MB-infected males on average mated two times more than the Microsporidia MB-uninfected F1 male mates from the age of 3-4 days to death (t = 2.2, df = 56.8, p = 0.03). Also, Microsporidia MB-infected males when combined in a cage with Microsporidia MB uninfected males were twice as competitive (χ² = 4.74, df = 1, p = 0.02) to the uninfected males in mating with uninfected females. In natural swarms, the proportion of Microsporidia MB-infected males was significantly higher compared to the non-swarming male mosquitoes (χ² = 685.5, df = 1, p < 0.0001).

There is a moderate, although heterogenous, horizontal transmission of Microsporidia MB across all age groups, except from 3-4 days old, infected females to males. Microsporidia MB-infected male mosquitoes were almost twice as competitive in mating as their uninfected counterparts. Therefore, Microsporidia MB infected males can potentially disseminate Microsporidia MB in the natural mosquito populations, thus, contributing to malaria control. However, semi-field studies are required to validate these results in a natural environment.