Molecular epidemiology of malaria prevalence and parasitaemia in a wild bird population

Abstract

Avian malaria (Plasmodium spp.) and other blood parasitic infections of birds constitute increasingly popular model systems in ecological and evolutionary host-parasite studies. Field studies of these parasites commonly use two traits in hypothesis testing: infection status (or prevalence at the population level) and parasitaemia, yet the causes of variation in these traits remain poorly understood. Here, we use quantitative PCR to investigate fine-scale environmental and host predictors of malaria infection status and parasitaemia in a large 4-year data set from a well-characterized population of blue tits (Cyanistes caeruleus). We also examine the temporal dynamics of both traits within individuals. Both infection status and parasitaemia showed marked temporal and spatial variation within this population. However, spatiotemporal patterns of prevalence and parasitaemia were non-parallel, suggesting that different biological processes underpin variation in these two traits at this scale. Infection probability and parasitaemia both increased with host age, and parasitaemia was higher in individuals investing more in reproduction (those with larger clutch sizes). Several local environmental characteristics predicted parasitaemia, including food availability, altitude, and distance from the woodland edge. Although infection status and parasitaemia were somewhat repeatable within individuals, infections were clearly dynamic: patent infections frequently disappeared from the bloodstream, with up to 26% being lost between years, and parasitaemia also fluctuated within individuals across years in a pattern that mirrored annual population-level changes. Overall, these findings highlight the ecological complexity of avian malaria infections in natural populations, while providing valuable insight into the fundamental biology of this system that will increase its utility as a model host-parasite system.

Maternal effects, malaria infections and the badge size of the house sparrow

“…Badge development probably depends on the condition of the bird at moult (Moreno-Rueda 2010) whereas infection may have occurred at any time until two weeks before the bird was caught (the limit of detection of malaria blood stages is generally two weeks post-infection; Valkiunas 2004). Some evidence suggests that wild birds are able to clear malaria infections (Knowles et al 2011), so if there really is a trade-off between badge size and malaria infection, it would be valuable to investigate the infection status at moult (i.e. in the late summer/autumn) and assess badge size the following year.…”

Mhc supertypes confer both qualitative and quantitative resistance to avian malaria infections in a wild bird population

“…Previous studies in this population on the closely related sympatric host species, blue tits (Cyanistes caeruleus), have shown that the two Plasmodium species differ substantially in their spatial distributions and impacts [15,35]. While P. circumflexum infections are associated with reduced survival, particularly during the acute stage of infection [15], P. relictum infections are linked with reproductive costs [14].…”

“…Breeding tits are territorial and forage in the vicinity of their nests [45]; hence, the nest-box coordinates give an accurate representation of an individual's location during and either side of the breeding season, when transmission is most likely [46]. Previous work on the Wytham Woods tit populations has shown that there is pronounced spatial variation in the distribution of the two Plasmodium species [34,35,47]. The local risk of infection with either P. relictum or P. circumflexum was obtained for each Mhc-typed great tit in 2008 and 2009 and calculated as the prevalence of infected great tits within a 500 m buffer (based on disease cluster distances obtained in Wood et al [34] and Lachish et al [47]) of the focal individuals' nest-box.…”

“…We predicted that the frequency of supertype 6 should be higher in older individuals, particularly in areas with elevated risk of infection, as a result of the selective disappearance of individuals that lack this supertype. We separated high-and low-infectionrisk areas by scoring whether an individual s nest-box was located within 500 m of the River Thames or not; P. circumflexum infection risk is substantially elevated in areas within 500 m of this large water body [34,35,47]. We assessed whether the frequency of the Mhc supertype varied as a function of host age (categorized as first year and older), and P. circumflexum infection risk, using a generalized linear model with binomial errors and a logit link, with both terms and their interaction included in the starting model.…”

“…First, risk of infection, particularly for vector-borne diseases, varies extensively at both large and small spatial scales [34][35][36]. Such factors, if not controlled for, may confound or conceal relevant patterns between Mhc and disease status [7].…”