Transstadial immune activation in a mosquito: Adults that emerge from infected larvae have stronger antibacterial activity in their hemocoel yet increased susceptibility to malaria infection

Abstract

Larval and adult mosquitoes mount immune responses against pathogens that invade their hemocoel. Although it has been suggested that a correlation exists between immune processes across insect life stages, the influence that an infection in the hemocoel of a larva has on the immune system of the eclosed adult remains unknown. Here, we used Anopheles gambiae to test whether a larval infection influences the adult response to a subsequent bacterial or malaria parasite infection. We found that for both female and male mosquitoes, a larval infection enhances the efficiency of bacterial clearance following a secondary infection in the hemocoel of adults. The adults that emerge from infected larvae have more hemocytes than adults that emerge from naive or injured larvae, and individual hemocytes have greater phagocytic activity. Furthermore, mRNA abundance of immune genes—such as cecropin A, Lysozyme C1, Stat‐A, and Tep1—is higher in adults that emerge from infected larvae. A larval infection, however, does not have a meaningful effect on the probability that female adults will survive a systemic bacterial infection, and increases the susceptibility of females to Plasmodium yoelii, as measured by oocyst prevalence and intensity in the midgut. Finally, immune proficiency varies by sex; females exhibit increased bacterial killing, have twice as many hemocytes, and more highly express immune genes. Together, these results show that a larval hemocoelic infection induces transstadial immune activation—possibly via transstadial immune priming—but that it confers both costs and benefits to the emerged adults.

Immune priming with inactive dengue virus during the larval stage of Aedes aegypti protects against the infection in adult mosquitoes

“…Tidbury et al 13 determined that 8 day-old Plodia interpunctella larvae, primed with a low dose of P. interpunctella granulosis virus, could survive a lethal virus challenge in the adult stage. Likewise, Brown et al 16 observed that Anopheles gambie adult mosquitoes from infected larvae have stronger antibacterial activity in their hemocoel. They also showed increased susceptibility to malaria infection.…”

“…development stages in insects [11][12][13][14][15][16] . On the other hand, it has been suggested that Ae.…”

Adult Mosquitoes Infected with Bacteria Early in Life Have Stronger Antimicrobial Responses and More Hemocytes after Reinfection Later in Life

“…In the present study, we uncovered that mosquitoes that receive two infections have more hemocytes available to quell the infection than mosquitoes that experience a single infection. Studies on E. coli -infected adult A. gambiae have documented an infection-induced increase in the number of hemocytes [ 35 , 37 , 44 , 45 ], and this increase extends to when mosquitoes acquire the E. coli infection during the larval stage and hemocytes are counted in adults [ 46 ]. Therefore, we predict that the surge in hemocytes associated with the initial infection—by the mitosis of circulating hemocytes [ 45 ]—carries over to strengthen the fight against the second infection.…”

“…We found a similar inverse correlation when studying cellular immunity in larvae and differently-aged adults; larvae have more hemocytes than adults but a smaller percentage of hemocytes engage in phagocytosis [ 37 ]. This contrasts with mosquitoes that were infected with E. coli as larvae and reinfected with E. coli as adults, where the number of hemocytes in mosquitoes infected twice was higher and so was their phagocytic activity [ 46 ]. This latter finding is similar to the strengthened phagocytosis response observed in mosquitoes treated with 20E [ 53 ].…”

“…In addition to an increase in hemocytes, mosquitoes infected twice expressed nitric oxide synthase ( NOS )—and perhaps prophenoloxidase 6 ( PPO6 )—more highly than mosquitoes that had been infected only once. Elevated expression of immune genes is associated with immune priming in mosquitoes [ 17 , 27 , 28 , 46 , 47 ], as well as in beetles and moths [ 56 , 57 , 58 ]. Particularly interesting is our finding that NOS is expressed more highly in mosquitoes infected twice.…”