Fitness effects of endemic malaria infections in a wild bird population: the importance of ecological structure

Abstract

Summary1. Parasites can have important effects on host populations influencing either fecundity or mortality, but understanding the magnitude of these effects in endemic host-parasite systems is challenging and requires an understanding of ecological processes affecting both host and parasite. 2. Avian blood parasites (Haemoproteus and Plasmodium) have been much studied, but the effects of these parasites on hosts in areas where they are endemic remains poorly known. 3. We used a multistate modelling framework to explore the effects of chronic infection with Plasmodium on survival and recapture probability in a large data set of breeding blue tits, involving 3424 individuals and 3118 infection diagnoses over nine years. 4. We reveal strong associations between chronic malaria infection and both recapture and survival, effects that are dependent on the clade of parasite, on host traits and on the local risk of infection. 5. Infection with Plasmodium relictum was associated with reduced recapture probability and increased survival, compared to P. circumflexum, suggesting that these parasites have differing virulence and cause different types of selection on this host. 6. Our results suggest a large potential survival cost of acute infections revealed by modelling host survival as a function of the local risk of infection. 7. Our analyses suggest not only that endemic avian malaria may have multiple fitness effects on their hosts and that these effects are species dependent, but also that adding ecological structure (in this case parasite species and spatial variation in disease occurrence) to analyses of host-parasite interactions is an important step in understanding the ecology and evolution of these systems.

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

“…prevent infection) would be beneficial to hosts that are exposed to more benign parasites, as these parasites are unlikely to cause mortality and are easier to suppress [53]. Using a multistate modelling framework, Lachish et al [15] showed that infection with P. circumflexum was associated with reduced survival in blue tits, compared with infection with P. relictum, suggesting that P. circumflexum is more virulent than P. relictum. In line with this finding, we found that uninfected great tits experienced lower survival rates in areas where P. circumflexum infection risk is high, suggesting a mortality cost for this parasite in great tits as well.…”

“…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].…”

“…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]. Here, we aimed to understand the role that Mhc play in determining host resistance and susceptibility to Plasmodium infections; and tested the three hypotheses that relate Mhc diversity to disease resistance: (i) the maximal diversity hypothesis; (ii) the optimal diversity hypothesis and (iii) effect of specific Mhc supertypes.…”

“…Thus, it is highly likely that the Mhc class I molecules of avian hosts recognize the peptides derived from malaria parasites and initiate cell destruction. Avian malaria parasites have been shown to compromise host fitness in both immunologically naive populations [12], as well as in species with which they are assumed to have shared a long evolutionary history [13][14][15], and are thus likely to exert strong selection on their hosts. These findings suggest that Mhc-linked malaria resistance should also exist in wild avian hosts, a premise supported by the results of several studies in passerine birds [16][17][18][19][20].…”

Local parasite lineage sharing in temperate grassland birds provides clues about potential origins of Galapagos avian Plasmodium

“…2005; Lachish et al. 2011), especially in cases where a host encounters a novel parasite (e.g., Atkinson and Samuel 2010; Bueno et al. 2010).…”