Do mosquitoes transmit the avian malaria-like parasite Haemoproteus? An experimental test of vector competence using mosquito saliva

Abstract

BackgroundThe life-cycle of many vector-borne pathogens includes an asexual replication phase in the vertebrate host and sexual reproduction in the insect vector. However, as only a small array of parasites can successfully develop infective phases inside an insect, few insect species are competent vectors for these pathogens. Molecular approaches have identified the potential insect vectors of blood parasites under natural conditions. However, the effectiveness of this methodology for verifying mosquito competence in the transmission of avian malaria parasites and related haemosporidians is still under debate. This is mainly because positive amplifications of parasite DNA in mosquitoes can be obtained not only from sporozoites, the infective phase of the malaria parasites that migrate to salivary glands, but also from different non-infective parasite forms in the body of the vector. Here, we assessed the vectorial capacity of the common mosquito Culex pipiens in the transmission of two parasite genera.MethodsA total of 1,560 mosquitoes were allowed to feed on five house sparrows Passer domesticus naturally infected by Haemoproteus or co-infected by Haemoproteus/Plasmodium. A saliva sample of the mosquitoes that survived after 13 days post-exposure was taken to determine the presence of parasite DNA by PCR.ResultsOverall, 31.2% mosquito’s head-thorax and 5.8% saliva samples analysed showed positive amplifications for avian malaria parasites. In contrast to Haemoproteus DNA, which was not found in either the body parts or the saliva, Plasmodium DNA was detected in both the head-thorax and the saliva of mosquitoes. Parasites isolated from mosquitoes feeding on the same bird corresponded to the same Plasmodium lineage.ConclusionsOur experiment provides good evidence for the competence of Cx. pipiens in the transmission of Plasmodium but not of Haemoproteus. Molecular analyses of saliva are an effective method for testing the vector competence of mosquitoes and other insects in the transmission of vector-borne pathogens.

Culex pipiens forms and urbanization: effects on blood feeding sources and transmission of avian Plasmodium

“…As occurred here, previous studies have reported the presence of Haemoproteus in mosquitoes [22, 34, 35, 37, 55], however experimental evidence available exclude mosquitoes as vectors of this parasite genus [31, 56]. The Haemoproteus passeris lineage Padom05 was isolated from a mosquito with a recent blood meal on a house sparrow, which is a common avian host of this parasite lineage [31, 57]. This, together with the fact that the mosquito had a recent blood meal from this bird species, suggests that the Haemoproteus DNA derived from rests of undigested blood present in the head-thorax of the mosquito.…”

“…Avian Plasmodium is a mosquito-borne parasite while the related Haemoproteus is mainly transmitted by Culicoides and louse flies [26]. As occurred here, previous studies have reported the presence of Haemoproteus in mosquitoes [22, 34, 35, 37, 55], however experimental evidence available exclude mosquitoes as vectors of this parasite genus [31, 56]. The Haemoproteus passeris lineage Padom05 was isolated from a mosquito with a recent blood meal on a house sparrow, which is a common avian host of this parasite lineage [31, 57].…”

“…This, together with the fact that the mosquito had a recent blood meal from this bird species, suggests that the Haemoproteus DNA derived from rests of undigested blood present in the head-thorax of the mosquito. Alternatively, it is possible that a non-infective form of the parasite present in the mosquito head-thorax was amplified [56], but see [31]. Although molecular isolation does not demonstrate vector competence, the Plasmodium parasites isolated from mosquitoes suggest that the two mosquito forms and their hybrids may frequently interact with birds infected by avian malaria parasites.…”

“…Furthermore, avian Plasmodium parasites, including P. relictum , successfully develops in Cx. p. pipiens as supported by experimental infections of mosquitoes [17, 29–31], and different avian Plasmodium lineages have been molecularly isolated from mosquitoes trapped in the wild [32–37]. …”

Louse flies of Eleonora’s falcons that also feed on their prey are evolutionary dead‐end hosts for blood parasites

“…The success of transmission of a particular parasite lineage to a new host depends to a large extent upon the susceptibility of the host and compatibility between blood‐feeding insects and parasite lineages (Beerntsen, James, & Christensen, ; Martínez‐de la Puente, Martínez, Rivero‐de Aguilar, Herrero, & Merino, ). Indeed, only a fraction of the parasites that are in contact with potential vectors are effectively transmitted (Gutiérrez‐López et al, ), because this process may be hampered by environmental, behavioral, genetic, and physiological factors that inhibit the development of parasites in blood‐sucking insects (Beerntsen et al, ; Molina‐Cruz, Garver et al, ). For example, the immune system of the human malaria vector Anopheles gambiae is able to eliminate some strains of Plasmodium falciparum , while other strains can evade this immune barrier through the function of a particular parasite gene (Molina‐Cruz et al, ; Molina‐Cruz, Garver et al, ).…”