Transstadial transmission of larval hemocoelic infection negatively affects development and adult female longevity in the mosquito Anopheles gambiae

Abstract

During all life stages, mosquitoes are exposed to pathogens, and employ an immune system to resist or limit infection. Although much attention has been paid to how adult mosquitoes fight infection, little is known about how an infection during the larval stage affects the biology of the resultant adult. In this study, we investigated whether a bacterial infection in the hemocoel of the African malaria mosquito, Anopheles gambiae, is transstadially transmitted from larvae to adults (both females and males), and whether immune stimulation in the hemocoel as a larva alters development or biological traits of the adult. Specifically, larvae were injected in the hemocoel with either fluorescent microspheres or Escherichia coli, and the following traits were examined: transstadial transmission, larval development to adulthood, adult survival, and adult body size. Our results show that transstadial transmission of hemocoel contents occurs from larvae to pupae and from pupae to adults, but that bacterial prevalence and intensity varies with age. Injury, immune stimulation or infection decreases the proportion of larvae that undergo pupation and eclosion, infection decreases the longevity of adult females, and treatment has complex effects on the body size of the resultant adults. The present study adds larval hemocoelic infection to the known non-genetic factors that reduce overall fitness by negatively affecting development and adult biological traits that influence mosquito vector competence.

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

“…In addition to changes in the abundance of hemocytes, variation in immune proficiency may arise from differences in the frequency or degree to which hemocytes phagocytose invaders (League et al, ). Because transstadial transmission of hemocoel infections occurs from larvae to adults (Brown et al, ), we first examined untreated adults that eclosed from E. coli ‐infected larvae. By means of fluorescence microscopy, we could not detect transstadially transmitted E. coli within the hemocytes of these mosquitoes; only a dim fluorescent haze without structural definition was observed in fewer than 10% of the hemocytes.…”

“…Taken together, larval exposure to certain microorganisms, be it in the gut or hemocoel, can boost the immune system of an adult mosquito. The underlying drivers behind this enhanced immunity remain largely unknown, but a larval hemocoelic infection can be transstadially passaged to adults, which may increase immune alertness due to a persistent infection (Brown et al, ). This idea is further supported by our finding that a larval challenge with an undegradable immune elicitor (microspheres) increases bacterial clearance in adults, whereas larval challenge with a degradable immune elicitor (heat‐killed E. coli ) does not.…”

“…The reason behind the lack of an obvious survival benefit for females is not clear, but it is possible that the effect of the larval infection is masking the protection conferred to adults. We recently reported that a larval infection negatively impacts the survival of untreated adults (Brown et al, ). Thus, the baseline survival is lower in adult mosquitoes that encountered an infection as larvae, and hence, a larval infection could be providing a modicum of protection against an adult infection but in this experiment this effect is undetectable.…”

“…Finally, the phenotype observed here is often considered to be a consequence of immune priming, and in this specific case, transstadial immune priming. Although transstadial immune priming may be occurring, we know that a hemocoelic bacterial infection is transstadially transmitted to the adults (Brown et al, ). Thus, we elected to instead refer to the phenotype observed here as transstadial immune activation because immune priming, in its strictest sense, involves the challenge of a quiescent immune system that has been primed in the past (Melillo et al, ).…”

“…Consequently, mosquito larvae mount powerful cellular and humoral immune responses against pathogens in their hemocoel (Biron et al, ; Dimopoulos, Richman, Muller, & Kafatos, ; Duncan et al, ; Kalucy & Daniel, ; League et al, ; League & Hillyer, ; Meredith, Hurd, Lehane, & Eggleston, ; Richman et al, ; Shin et al, ). Recently, we demonstrated that a larval‐acquired infection in the hemocoel is transstadially transmitted to the hemocoel of an adult, which may have important implications for adult immunity (Brown, Thompson, & Hillyer, ). We hypothesize that a larval‐acquired infection activates the immune system such that the resultant adult is better able to respond to a future infection.…”