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Plasmodiumparasites that cause bird malaria occur in all continents except Antarctica and are primarily transmitted by mosquitoes in the genusCulex.Culex quinquefasciatus, the mosquito vector of avian malaria in Hawaiʻi, became established in the islands in the 1820s. While the deadly effects of malaria on endemic bird species have been documented for many decades, vector-parasite interactions in avian malaria systems are relatively understudied.

To evaluate the gene expression response of mosquitoes exposed to aPlasmodiuminfection intensity known to occur naturally in Hawaiʻi, offspring of wild-collected HawaiianCx. quinquefasciatuswere fed on a domestic canary infected with a fresh isolate ofPlasmodium relictumGRW4 from a wild-caught Hawaiian honeycreeper. Control mosquitoes were fed on an uninfected canary. Transcriptomes of five infected and three uninfected individual mosquitoes were sequenced at each of three stages of the parasite life cycle: 24 h post feeding (hpf) during ookinete invasion; 5 days post feeding (dpf) when oocysts are developing; 10 dpf when sporozoites are released and invade the salivary glands.

Differential gene expression analyses showed that during ookinete invasion (24 hpf), genes related to oxidoreductase activity and galactose catabolism had lower expression levels in infected mosquitoes compared to controls. Oocyst development (5 dpf) was associated with reduced expression of a gene with a predicted innate immune function. At 10 dpf, infected mosquitoes had reduced expression levels of a serine protease inhibitor, and further studies should assess its role as aPlasmodiumagonist inC. quinquefasciatus. Overall, the differential gene expression response of HawaiianCulexexposed to aPlasmodiuminfection intensity known to occur naturally in Hawaiʻi was low, but more pronounced during ookinete invasion.

This is the first analysis of the transcriptional responses of vectors to malaria parasites in non-mammalian systems. Interestingly, few similarities were found between the response ofCulexinfected with a birdPlasmodiumand those reported inAnophelesinfected with humanPlasmodium. The relatively small transcriptional changes observed in mosquito genes related to immune response and nutrient metabolism support conclusions of low fitness costs often documented in experimental challenges ofCulexwith avianPlasmodium.