Quantitative trait loci in Anopheles gambiae controlling the encapsulation response against Plasmodium cynomolgi Ceylon

Abstract

Background: Anopheles gambiae females are the world's most successful vectors of human malaria. However, a fraction of these mosquitoes is refractory to Plasmodium development. L3-5, a laboratory selected refractory strain, encapsulates transforming ookinetes/early oocysts of a wide variety of Plasmodium species. Previous studies on these mosquitoes showed that one major (Pen1) and two minor (Pen2, Pen3) autosomal dominant quantitative trait loci (QTLs) control the melanotic encapsulation response against P. cynomolgi B, a simian malaria originating in Malaysia.

Results: We have investigated the response of L3-5 to infection with P. cynomolgi Ceylon, a different but related parasite species, in crosses with the susceptible strain 4Arr. Refractoriness to this parasite is incompletely recessive. Infection and genotyping of F2 intercross females at genome-spanning microsatellite loci revealed that 3 autosomal QTLs control encapsulation of this species. Two loci map to the regions containing Pen2 and Pen3. The novel QTL maps to chromosome 3R, probably to polytene division 32 or 33. Thus the relative contribution of any QTL to oocyst encapsulation varies with the species of parasite. Further, different QTLs were most readily identified in different F2 families. This, like the F1 data, suggests that L3-5 is not genetically homogeneous and that somewhat different pathways may be used to achieve an encapsulation response.

Conclusion: We have shown here that different QTLs are involved in responses against different Plasmodium parasites.

Figure 1

Melanotic encapsulation of P. cynomolgi Ceylon by A. gambiae. (A) Responses of individual parental L3-5 refractory strain (squares and circles) and 4Arr susceptible strain females (diamonds and triangles) to P. cynomolgi Ceylon infection. Exp.1 and exp. 2 indicate two separate infection experiments. (B) Responses of F1 female progeny from one cross between L3-5 females and 4Arr males (closed diamonds) and three crosses between 4Arr females and L3-5 males (open squares, circles and triangles).

Figure 2

P. cynomolgi Ceylon infection phenotypes of F2 female progeny from crosses of six F1 females with their sibling males. (A) Intensity of infection was plotted against the total number of oocysts, both normal and encapsulated, per female midgut. N = 167. (B) Encapsulation responses of 123 infected F2 females. The number of F2 females was plotted against the fraction of oocysts encapsulated per midgut.