Stress dependent infection cost of the human malaria agent Plasmodium falciparum on its natural vector Anopheles coluzzii

Abstract

Unraveling selective forces that shape vector-parasite interactions has critical implications for malaria control. However, it remains unclear whether Plasmodium infection induces a fitness cost to their natural mosquito vectors. Moreover, environmental conditions are known to affect infection outcome and may impact the effect of infection on mosquito fitness. We investigated in the laboratory the effects of exposition to and infection by field isolates of Plasmodium falciparum on fecundity and survival of a major vector in the field, Anopheles coluzzii under different conditions of access to sugar resources after blood feeding. The results evidenced fitness costs induced by exposition and infection. When sugar was available after blood meal, infected and exposed mosquitoes had either reduced or equal to survival to unexposed mosquitoes while fecundity was either increased or decreased depending on the blood donor. Under strong nutritional stress, survival was reduced for exposed and infected mosquitoes in all assays. We therefore provide here evidence of an environmental-dependant reduced survival in mosquitoes exposed to infection in a natural and one of the most important parasite-mosquito species associations for human malaria transmission.

Larval nutritional stress affects vector life history traits and human malaria transmission

“…However, while we observed greater survival rates in infected mosquitoes, the number of eggs produced was not significantly different from unexposed females which suggest that this trade-off might not be at play here. Finally, we observed a strong interaction between gametocyte carrier and female infection status in the survival assays as previously observed in sugar-stressed females41 which might be due to the parasite’s genetic factors (e.g. infection intensity, multiplicity of infection) or to blood quality (e.g.…”

“…Contrasting results on mosquito survival rates are found in malaria parasite - mosquito systems with greater survival rates for individuals infected with Plasmodium relictum accompanied by a reduction in fecundity40 and a lower survival rate for individuals infected with P . falciparum without any indication of a fecundity trade-off41. In addition, the hypothesis of host manipulation by parasites suggests that a malaria parasite might enhance its host’s survival to increase transmission4042.…”

Larval diet affects mosquito development and permissiveness to Plasmodium infection

“…FP-fed larvae produced highly permissive mosquitoes that survived longer after Plasmodium infection than the controls fed on FF, whereas feeding on D did not affect adult permissiveness to Plasmodium infection or survival. Although an increase in survival might be surprising with an increased infection load, Plasmodium infection is known not to inflict much of a fitness cost on mosquitoes in the absence of nutritional stress38, as is the case for our mosquitoes fed with fructose ad libitum . Thus, our results point to FP mosquitoes being fitter, thus either allowing a higher Plasmodium infection or surviving it better.…”

Evolutionary potential of the extrinsic incubation period of dengue virus inAedes aegypti

“…) and interactions with the environment (Ferguson and Read ; Sangare et al. ). Our growing appreciation for the diverse and specialized immune response of insects (Sim et al.…”

“…While previously assumed to be mostly benign (Hardy et al 1983), vector responses to pathogens are governed by the same constraints as host/parasite relationships; balancing the need to invest in an immune response against the costs of any pathogen induced virulence (McKean and Lazzaro 2011). Pathogen infections can negatively affect vector fitness but the magnitude of the impact seems to vary depending on mosquito genotype (Maciel-de-Freitas et al 2011;Carrington et al 2013;Sylvestre et al 2013;Hill et al 2014) and interactions with the environment (Ferguson and Read 2002;Sangare et al 2014). Our growing appreciation for the diverse and specialized immune response of insects (Sim et al 2014), typically revealed by transcriptional profiling (Oduol et al 2000;Bonizzoni et al 2012), offers an independent means to assess the nature of a vector's energetic investment in pathogen interactions (Ye et al 2009).…”