Variation in susceptibility to parasite infection: patterns, determinants and consequences in red-fronted lemurs

Parasites and infectious diseases represent an ecological force shaping animal social evolution. Particular attention has been paid to parasite infection as a driver of mate choice in models of sexual selection as one sex may advertise parasite resistance via elaborate sexual selected phenotypic signals. Although empirical studies supporting the importance of parasite infection in natural populations abound in various vertebrate orders, relatively little is known about both dynamics and impact of parasite infections and infectious diseases in natural populations of primates. More specifically, there is a particular lack of baseline parasitological information in strepsirrhine primate species. Using an interdisciplinary approach that combined individual parasite, genetic, hormone and sociobiological information, I studied patterns and proximate determinants of gastro-intestinal parasite susceptibility in a wild population of red-fronted lemurs (Eulemur fulvus rufus). Male red-fronted lemurs display a more conspicuous facial colouration than females do and there is considerable inter-individual variation in this trait among males. In a second step, I examined if strong parasite infections have negative consequences on male reproductive and whether male colourations is a condition-dependent ornament that can be provide information on male quality. During two 4-month field studies in 2006 and 2007, I collected several types of data on 29 adult individually marked male and female lemurs in Kirindy Forest, western Madagascar. Data on parasite infection and hormone levels were obtained by analysing faecal samples that were collected non-invasively once per week. Data on mating and reproductive success were obtained through focal animal observations and genetic paternity analyses. The entire population was infected by a minimum of 10 unique parasite species including 8 helminth and 2 protozoa species. Prevalence of the majority of parasite infection and parasite species richness was higher than ever recorded from other lemur species. The four social groups studied differed partially in their parasite fauna, which was probably due to minor differences in habitat parameters. Comparisons to other lemur studies indicated that long-term studies, such as conducted during this project, might provide a better estimate of parasite infection than short-term studies. Part of individual variability in parasite infection could be explained by a newly detected genetic polymorphism in the IL4 gene promoter that regulates immune response against nematode infections and facilitates worm expulsion. Carriers of a particular genotype showed highest nematode infection intensities, suggesting a functional role of the IL4 polymorphism, yet individual reproductive success appeared not impaired and long-term population analyses indicated higher reproductive success of these individuals than expected. Group size, age, sex and rank explained only a part of variation in parasite infection susceptibility on population level and lemur characteristic traits helped to understand detected patterns. Male mating and reproductive success were not correlated to any measure of parasite infection, which suggests a non-functional role of gastro-intestinal parasite in red-fronted lemur sexual selective processes. Additionally, male facial colouration, although under proximate control of androgens, did not appear to function as prominent predictor of reproductive success. The population was subject to strong seasonal variation in parasite infection levels between years, which was significantly associated to changes in androgen and glucocorticoid levels. Contrary to predictions of the immunocompetence hypothesis, which assumes immune-suppressive action of androgens, results indicate an immune-enhancing effect of androgen and glucocorticoid levels, leading to a decrease in parasite species richness and nematode infection intensity. Although the comprehensive approach applied in this thesis provided valuable new insights, I propose that additional factors such as body c ondition or nutrient supply but also information on parasite population dynamics need to be incorporated into future models in order to further improve our understanding of the multi-faceted interactions of primate hosts and parasites under natural conditions