Abstract
BackgroundThe immune system of adult mosquitoes has received significant attention because of the ability of females to vector disease-causing pathogens while ingesting blood meals. However, few studies have focused on the immune system of larvae, which, we hypothesize, is highly robust due to the high density and diversity of microorganisms that larvae encounter in their aquatic environments and the strong selection pressures at work in the larval stage to ensure survival to reproductive maturity. Here, we surveyed a broad range of cellular and humoral immune parameters in larvae of the malaria mosquito, Anopheles gambiae, and compared their potency to that of newly-emerged adults and older adults.ResultsWe found that larvae kill bacteria in their hemocoel with equal or greater efficiency compared to newly-emerged adults, and that antibacterial ability declines further with adult age, indicative of senescence. This phenotype correlates with more circulating hemocytes and a differing spatial arrangement of sessile hemocytes in larvae relative to adults, as well as with the individual hemocytes of adults carrying a greater phagocytic burden. The hemolymph of larvae also possesses markedly stronger antibacterial lytic and melanization activity than the hemolymph of adults. Finally, infection induces a stronger transcriptional upregulation of immunity genes in larvae than in adults, including differences in the immunity genes that are regulated.ConclusionsThese results demonstrate that immunity is strongest in larvae and declines after metamorphosis and with adult age, and suggest that adaptive decoupling, or the independent evolution of larval and adult traits made possible by metamorphosis, has occurred in the mosquito lineage.
Highlights
The immune system of adult mosquitoes has received significant attention because of the ability of females to vector disease-causing pathogens while ingesting blood meals
We show that mosquito larvae are more proficient than adults in killing bacteria, and that this correlates with stronger cellular and humoral immune responses in larvae compared to adults
This difference in antibacterial activity was due to an induced response, rather than a constitutive response, as the antibacterial activity in the hemolymph of naïve and injured individuals did not differ between larvae and adults, with the exception of when injured larvae were compared to 1-day-old adults (Šidák’s: P = 0.0387). To test whether this finding was unique to immune stimulation with Gram (−) E. coli, we repeated the experiment by stimulating mosquitoes with heat-killed Gram (+) M. luteus (Fig. 5c, d) and heatkilled Gram (−) Enterobacter sp. isolate Ag1 (Fig. 5e-f ), a bacterial strain that naturally colonizes the midgut of A. gambiae and is a core adult bacterial symbiont taxon [43, 44]. In both sets of experiments, antibacterial activity of hemolymph was significantly higher in larvae compared to adults (Fig. 5d, F; two-way Analysis of variance (ANOVA): F(2, 59) = 13.06, P < 0.0001 for M. luteus and F(2, 65) = 13.17, P < 0.0001 for Enterobacter sp.; Šidák’s: P ≤ 0.0252 for all comparisons)
Summary
The immune system of adult mosquitoes has received significant attention because of the ability of females to vector disease-causing pathogens while ingesting blood meals. Mosquitoes face the threat of infection during all stages of their holometabolous life cycle These threats arise from numerous sources, including the microbe-rich aquatic environments where larvae reside and the infected blood meals that adults ingest. To combat pathogens that invade their hemocoel (body cavity), mosquitoes have evolved a diverse array of cellular and humoral immune responses [1]. These responses begin when pathogenassociated molecular patterns are recognized by host-. This recognition triggers the amplification or repression of extracellular signaling cascades, the initiation of intracellular signal transduction pathways and, the activation or expression of immune effectors. These immune effectors, together with the circulating and sessile hemocytes (insect blood cells) that produce many of them, kill pathogens via phagocytosis, lysis, melanization, and other mechanisms [2, 3]
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