LIVING WITH PARASITES: AVIAN MALARIA, TELOMERE LENGTH AND LIFE HISTORY TRADE-OFFS

Abstract: Haemosporidia is a well-studied group of parasites, which infect mammals, reptiles and birds and use blood sucking vectors for their transmission. By conducting natural population studies and experimental infections, We have been able to detect and quantify Haemosporidia from avian blood to investigate how these pathogens affect their avian hosts. We have used life history data of two long-term longitudinal studies of wild bird populations: great reed warbler, Acrocephalus arundinaceus (25 year data) and house martin, Delichon urbica (10 year data) to investigate the relationships between parasite prevalence and parasitemia and host life history traits. By conducting experimental infections in great reed warblers, we demonstrated that the acute phase parasitemia of the avian malaria Plasmodium ashfordi (GRW2) is significantly positively correlated to the subsequent chronic infection level. We outlined a framework of how candidate Major Histocompatibility Complex (MHC) alleles are associated with infectious diseases in natural populations of animal. We proposed that three types of MHC alleles (qualitative disease resistance, quantitative disease resistance and susceptibility alleles) could be separated by combining data of prevalence and intensity (parasitemia). We tested our hypothesis in a long-term longitudinal data set of great reed warblers, and found a MHC class-I allele (B4b) that was both positively associated with prevalence of severe malaria infection (GRW2) and negatively correlated with GRW2 parasitemia, a pattern typical for a quantitative resistance allele. Using longitudinal data of great reed warblers, we found that telomere length in great reed warblers is maternally inherited and offspring telomere length is associated with their mother`s age. By using our full pedigree (25 year) great reed warbler data, we found that both early life (at day 9) telomere length and malaria infections (at 1 year age) significantly predicted the individual`s lifespan. Moreover, we found that birds infected with malaria parasites lost significantly more of their telomeres during the first year of life. These results are supported by data from our experimental infection study, where birds infected with the GRW2 parasite showed a higher telomere loss than control birds. Furthermore, we found that parasitemia was positively correlated with telomere loss rate in both natural population (GRW2 and GRW4 parasitemia) and experimental infection (GRW2 parasitemia). Taken together, because malaria parasites increase the telomere attrition rate of the host, it provides a mechanistic explanation for the underlying physiological processes that link the negative effect of a parasite infection to cell ageing and host survival.