Abstract
The utility of using evolutionary and ecological frameworks to understand the dynamics of infectious diseases is gaining increasing recognition. However, integrating evolutionary ecology and infectious disease epidemiology is challenging because within-host dynamics can have counterintuitive consequences for between-host transmission, especially for vector-borne parasites. A major obstacle to linking within- and between-host processes is that the drivers of the relationships between the density, virulence, and fitness of parasites are poorly understood. By experimentally manipulating the intensity of rodent malaria (Plasmodium berghei) infections in Anopheles stephensi mosquitoes under different environmental conditions, we show that parasites experience substantial density-dependent fitness costs because crowding reduces both parasite proliferation and vector survival. We then use our data to predict how interactions between parasite density and vector environmental conditions shape within-vector processes and onward disease transmission. Our model predicts that density-dependent processes can have substantial and unexpected effects on the transmission potential of vector-borne disease, which should be considered in the development and evaluation of transmission-blocking interventions.
Highlights
The density of individuals within a shared environment is a key factor in determining fitness, shaping both ecological and evolutionary processes (MacArthur and Wilson 1967; Mueller et al 1991; Bassar et al 2010)
This difference is partly explained by slightly higher gametocyte densities in high density’ (HD) than regular density’ (RD) infections in mice used for setting up cultures (mean number of gametocytes per mL of blood: RD = 1.10 9 1010 (Æ 8.57 9 SE); HD = 1.86 9 1010 (Æ 1.14 9 SE); v21 = 5.81, P = 0.016) and an almost two-fold greater fertilization rate in the HD line (ookinete density/female gametocyte density: RD = 3.5 9 10À3 (Æ 4.5 9 10À4 SE); HD = 6.6 x 10-3(Æ 4.4 9 10À4 SE); v21 = 6.436, P = 0.0112)
Having confirmed that the HD line resulted in significantly higher numbers of ookinetes and oocysts than the RD line, we examined parasite proliferation, measured by the density of sporozoites successfully reaching the salivary glands
Summary
The density of individuals within a shared environment is a key factor in determining fitness, shaping both ecological and evolutionary processes (MacArthur and Wilson 1967; Mueller et al 1991; Bassar et al 2010). Interactions between different forms of competition and environmental variation complicate efforts to understand the link between density dependence and evolutionary and ecological processes (Begon et al 2005; Aboagye-Antwi et al 2010). This is because identifying the life-history stages and demographic factors that are most sensitive to density dependence is often very difficult (Bassar et al.2010). For microparasitic vector-borne diseases, how the density of parasites within the host influences within-vector processes and onwards transmission to
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