Social interactions modulate the virulence of avian malaria infection

Abstract

34There is an increasing understanding of the context-dependent nature of parasite 35 virulence. Variation in parasite virulence can occur when infected individuals compete with 36 conspecifics that vary in infection status; virulence may be higher when competing with 37 uninfected competitors. In vertebrates with social hierarchies, we propose that these 38 competition-mediated costs of infection may also vary with social status. Dominant 39 individuals have greater competitive ability than competing subordinates, and consequently 40 may pay a lower prevalence-mediated cost of infection. In this study we investigated whether 41 costs of malarial infection were affected by the occurrence of the parasite in competitors and 42 social status in domestic canaries (Serinus canaria). We predicted that infected subordinates 43 competing with non-infected dominants would pay higher costs than infected subordinates 44 competing with infected dominants. We also predicted that these occurrence-mediated costs 45 of infection would be ameliorated in infected dominant birds. We found that social status and 46 the occurrence of parasites in competitors significantly interacted to change haematocrit in 47 infected birds. Namely, subordinate and dominant infected birds differed in haematocrit 48 depending on the infection status of their competitors. However, in contrast to our prediction 49 dominants fared better with infected subordinates, whereas subordinates fared better with 50 uninfected dominants. Moreover, we found additional effects of parasite occurrence on 51 mortality in canaries. Ultimately, we provide evidence for costs of parasitism mediated by 52 social rank and the occurrence of parasites in competitors in a vertebrate species. This has 53 important implications for our understanding of the evolutionary processes that shape parasite 54 virulence and group living. 55

Indirect effects of parasitism: costs of infection to other individuals can be greater than direct costs borne by the host

“…The importance of indirect effects has previously been demonstrated between hosts and non-hosts of different species and of the same species even where there is little contact between family members [4,6]. However, Larcombe et al [4] recently highlighted that such effects could be mediated by the social relationships between individuals in a group, with dominance status playing a key role in the impact of parasitism both on host traits related to fitness and parasite traits related to virulence. Family relationships are likely to play a stronger role, particularly in species with parental care, as individuals are related.…”

“…While it is becoming widely recognized that the social environment in which parasitism occurs is key to both host and parasite fitness, the integration of indirect effects to these studies has received less attention. The importance of indirect effects has previously been demonstrated between hosts and non-hosts of different species and of the same species even where there is little contact between family members [4,6]. However, Larcombe et al [4] recently highlighted that such effects could be mediated by the social relationships between individuals in a group, with dominance status playing a key role in the impact of parasitism both on host traits related to fitness and parasite traits related to virulence.…”

“…The costs of parasitism at this time may therefore have a substantial impact on social dynamics by altering how resources are partitioned between group members [8,9]. While social interactions are known to play a major role in the spread of infection [10] and can influence host and non-host responses to infection in experimental settings [4], the relative impact of direct and indirect effects of parasitism on host traits in wild populations remains unclear.…”

“…There is increasing recognition that infection can also alter the way that hosts interact and share resources with other individuals in their social environment [2,3]. This can lead to additional, indirect costs of infection for individuals with which the host interacts, for example by altering host success in competitive interactions or influencing how hosts use or contribute to group resources [2][3][4][5][6]. The impact of both direct and indirect effects of parasitism are likely to become particularly acute during periods of reproduction, when adult and juvenile hosts are under additional nutritional stress and relatives may share limited resources.…”

“…to play a major role in the spread of infection [10] and can influence host and non-host responses to infection in experimental settings [4], the relative impact of direct and indirect effects of parasitism on host traits in wild populations remains unclear.…”