A mating-induced reproductive gene promotes Anopheles tolerance to Plasmodium falciparum infection.

Perrine Marcenac,Evdoxia G Kakani,Abdoulaye Diabaté,Rakiswendé Serge Yerbanga,Kristine Werling,Adam South,Sara N Mitchell,Thierry Lefèvre,Flaminia Catteruccia,Eryney Marrogi,Roch K Dabiré,Daniel G Abernathy,W Robert Shaw

doi:10.1371/journal.ppat.1008908

Perrine Marcenac, Evdoxia G Kakani + Show 11 more

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https://doi.org/10.1371/journal.ppat.1008908

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Abstract

Anopheles mosquitoes have transmitted Plasmodium parasites for millions of years, yet it remains unclear whether they suffer fitness costs to infection. Here we report that the fecundity of virgin and mated females of two important vectors-Anopheles gambiae and Anopheles stephensi-is not affected by infection with Plasmodium falciparum, demonstrating that these human malaria parasites do not inflict this reproductive cost on their natural mosquito hosts. Additionally, parasite development is not impacted by mating status. However, in field studies using different P. falciparum isolates in Anopheles coluzzii, we find that Mating-Induced Stimulator of Oogenesis (MISO), a female reproductive gene strongly induced after mating by the sexual transfer of the steroid hormone 20-hydroxyecdysone (20E), protects females from incurring fecundity costs to infection. MISO-silenced females produce fewer eggs as they become increasingly infected with P. falciparum, while parasite development is not impacted by this gene silencing. Interestingly, previous work had shown that sexual transfer of 20E has specifically evolved in Cellia species of the Anopheles genus, driving the co-adaptation of MISO. Our data therefore suggest that evolution of male-female sexual interactions may have promoted Anopheles tolerance to P. falciparum infection in the Cellia subgenus, which comprises the most important malaria vectors.

Highlights

Parasites of the genus Plasmodium are the causative agents of malaria, a disease that infects hundreds of millions and kills over 400,000 people, mostly children, every year [1]
Plasmodium falciparum, the deadliest form of human malaria, is transmitted when female Anopheles mosquitoes bite people and take a blood meal in order to develop eggs. It is still poorly understood whether Anopheles mosquitoes that get infected with P. falciparum suffer fitness costs
We unexpectedly found that egg numbers were positively correlated with P. falciparum infection intensity, so that females that produced more eggs in their ovaries harbored greater parasite numbers in their midgut

Summary

Introduction

Parasites of the genus Plasmodium are the causative agents of malaria, a disease that infects hundreds of millions and kills over 400,000 people, mostly children, every year [1]. Cellia species from the African continent have been vectors of Plasmodium falciparum, the deadliest malaria parasite, for the last 10,000–50,000 years [5,6,7,8], and have transmitted ancestral Plasmodium species for millions of years [9] Given their long-term association with P. falciparum and its ancestral forms, an intriguing question is whether these vectors suffer fitness costs to infection. We and others have found that parasites can utilize lipids carried by the mosquito lipid transporter lipophorin for their own growth [17,20,21], but they do so without impairing egg development [17] These results suggest a non-competitive P. falciparum developmental strategy tailored to An. gambiae reproductive biology [17], the study used virgin females and did not determine the full costs potentially inflicted by parasites in reproductively active, mated females

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