Mosquito age and avian malaria infection

Abstract

BackgroundThe immune system of many insects wanes dramatically with age, leading to the general prediction that older insects should be more susceptible to infection than their younger counterparts. This prediction is however challenged by numerous studies showing that older insects are more resistant to a range of pathogens. The effect of age on susceptibility to infections is particularly relevant for mosquitoes given their role as vectors of malaria and other diseases. Despite this, the effect of mosquito age on Plasmodium susceptibility has been rarely explored, either experimentally or theoretically.MethodsExperiments were carried out using the avian malaria parasite Plasmodium relictum and its natural vector in the field, the mosquito Culex pipiens. Both innate immune responses (number and type of circulating haemocytes) and Plasmodium susceptibility (prevalence and burden) were quantified in seven- and 17-day old females. Whether immunity or Plasmodium susceptibility are modulated by the previous blood feeding history of the mosquito was also investigated. To ensure repeatability, two different experimental blocks were carried out several weeks apart.ResultsHaemocyte numbers decrease drastically as the mosquitoes age. Despite this, older mosquitoes are significantly more resistant to a Plasmodium infection than their younger counterparts. Crucially, however, the age effect is entirely reversed when old mosquitoes have taken one previous non-infected blood meal.ConclusionsThe results agree with previous studies showing that older insects are often more resistant to infections than younger ones. These results suggest that structural and functional alterations in mosquito physiology with age may be more important than immunity in determining the probability of a Plasmodium infection in old mosquitoes. Possible explanations for why the effect is reversed in blood-fed mosquitoes are discussed. The reversal of the age effect in blood fed mosquitoes implies that age is unlikely to have a significant impact on mosquito susceptibility in the field.Electronic supplementary materialThe online version of this article (doi:10.1186/s12936-015-0912-z) contains supplementary material, which is available to authorized users.

Insect immunology and hematopoiesis

“…Such observations have been made in Diptera, Hymenoptera, Lepidoptera, Coleoptera, and Odonata. Often, senescence refers to a decrease in the potency of a response that involves encapsulation, nodulation or melanization (Daukste et al, 2012; Park et al, 2011; Prasai and Karlsson, 2012; Robb and Forbes, 2006), or refers to a decrease in the number of hemocytes or their phagocytic activity (Hillyer et al, 2005; Horn et al, 2014; Mackenzie et al, 2011; Park et al, 2011; Pigeault et al, 2015; Schmid et al, 2008). This senescence often results in increased infection intensities in older insects, which may be accompanied by either increased (Roberts and Hughes, 2014) or decreased (Hillyer et al, 2005) survival.…”

“…This senescence often results in increased infection intensities in older insects, which may be accompanied by either increased (Roberts and Hughes, 2014) or decreased (Hillyer et al, 2005) survival. Seemingly conflicting with the concept of immunosenescence, reports on insect vectors have demonstrated that older flies are less capable of becoming infected with – and transmitting – malaria parasites, filarial nematodes, or the parasites that cause human African trypanosomiasis (Aksoy et al, 2014; Ariani et al, 2015; Pigeault et al, 2015), indicating that the relationship between immunity, tolerance, and aging is complex.…”

Transmission traits of malaria parasites within the mosquito: Genetic variation, phenotypic plasticity, and consequences for control

“…Besides mosquito and parasite genetic factors, there is a great diversity of ways in which biotic and abiotic external and within‐vector environmental factors (temperature, mosquito diet, insecticide exposure, microbial gut flora, infection history, mosquito age, etc.) can influence with mosquito competence (Alout, Djègbè, et al., ; Gendrin et al., ; Hien et al., ; Lefèvre, Vantaux, Dabiré, Mouline, & Cohuet, ; Murdock, Blanford, Luckhart, & Thomas, ; Murdock, Paaijmans, Cox‐foster, Read, & Thomas, ; Pigeault, Nicot, Gandon, & Rivero, ; Pollitt, Bram, Blanford, Jones, & Read, ; Shapiro, Murdock, Jacobs, Thomas, & Thomas, ; Takken et al., ; Vantaux, Dabiré, Cohuet, & Lefèvre, ). However, it is still unknown whether these environmentally driven changes in competence illustrate mere passive susceptibilities to environmental stresses (nonadaptive plasticity) or active beneficial shifts in either parasite growth and development or mosquito immune responses (parasite or vector adaptive phenotypic plasticity; Box 2).…”

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

“…First, naïve larvae have more hemocytes than naïve adults (League et al, ). Second, the number of hemocytes in adult mosquitoes declines with age, a phenomenon that contributes to immune senescence (Castillo, Robertson, & Strand, ; Hillyer et al, ; King & Hillyer, ; League et al, ; Pigeault, Nicot, Gandon, & Rivero, ). However, an adult infection results in an increase in the number of hemocytes in some mosquito species but not others (Coggins et al, ; Hillyer et al, ; King & Hillyer, ; League et al, ).…”