Maina Tracy, Shisia Aclaine, Gichuhi Joseph, Bargul Joel L, Herren Jeremy K, Bukhari Tullu
Global Health Thematic Research Programme, International Centre of Insect Physiology and Ecology (Icipe), P.O. Box 30772 - 00100, Nairobi, Kenya.
Department of Biochemistry, Jomo Kenyatta University of Agriculture and Technology (JKUAT), P.O. Box, 62000 - 00200, Nairobi, Kenya.
Malar J. 2025 Apr 9;24(1):114. doi: 10.1186/s12936-025-05354-1.
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 (χ = 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 (χ = 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 (χ = 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.
微孢子虫MB是阿拉伯按蚊体内自然存在的一种共生体，可抑制疟原虫的发育。它可通过垂直和水平方式传播，从而在蚊虫种群中扩散。目前，交配是已知的唯一水平传播机制。了解交配过程中影响微孢子虫MB传播的因素对于制定基于这种共生体的疟疾传播阻断策略至关重要。
通过对三个年龄组（3 - 4天、7 - 8天和10 - 11天）的感染和未感染阿拉伯按蚊雌雄个体进行交配生物测定，确定蚊虫年龄对微孢子虫MB传播的影响。还进行了交配生物测定，以确定微孢子虫MB感染是否会影响雄蚊的个体交配频率和交配竞争力。为评估微孢子虫MB感染对野外条件下群聚的影响，收集了群聚和非群聚的阿拉伯按蚊雄蚊，并比较了它们的微孢子虫MB感染率。
蚊虫年龄不影响微孢子虫MB从雄蚊向雌蚊的传播（χ = 11.6，自由度 = 12，p = 0.47）。然而，在3 - 4日龄组中未观察到微孢子虫MB从雌蚊向雄蚊的传播。虽然存在异质性，但从雄蚊到雌蚊的总体传播率（41.5%）高于从雌蚊到雄蚊的传播率（22.4%）。当个体雄蚊（感染或未感染微孢子虫MB）与雌蚊交配时，从3 - 4日龄到死亡，感染微孢子虫MB的雄蚊平均交配次数比未感染微孢子虫MB的F1代雄蚊多两倍（t = 2.2，自由度 = 56.8，p = 0.03）。此外，将感染微孢子虫MB的雄蚊与未感染微孢子虫MB的雄蚊放在一个笼子里时，在与未感染雌蚊交配方面，感染微孢子虫MB的雄蚊比未感染的雄蚊竞争力强两倍（χ = 4.74，自由度 = 1，p = 0.02）。在自然群聚中，感染微孢子虫MB的雄蚊比例显著高于非群聚雄蚊（χ = 685.5，自由度 = 1，p < 0.0001）。
除了3 - 4日龄感染的雌蚊向雄蚊的传播外，微孢子虫MB在所有年龄组中都存在中等程度的、尽管是异质性的水平传播。感染微孢子虫MB的雄蚊在交配中的竞争力几乎是未感染雄蚊的两倍。因此，感染微孢子虫MB的雄蚊有可能在自然蚊虫种群中传播微孢子虫MB，从而有助于疟疾控制。然而，需要进行半野外研究以在自然环境中验证这些结果。
