Reduction in population size and not a shift in parasite community affect evolution of immune genes in island birds

Abstract

AbstractShared ecological conditions encountered by species that colonize islands often lead to the evolution of convergent phenotypes, commonly referred to as “island syndrome”. Reduced immune functions have been previously proposed to be part of the island syndrome, as a consequence of the reduced diversity of pathogens on island ecosystems. According to this hypothesis, immune genes are expected to exhibit genomic signatures of relaxed selection pressure in island species. In this study, we used comparative genomic methods to study immune genes in island species (N = 20) and their mainland relatives (N = 14). We gathered public data as well as generated new data on innate (Toll-Like Receptors, Beta Defensins) and acquired immune genes (Major Histocompatibility Complex classes I and II), but also on hundreds of genes annotated as involved in various immune functions. As a control, we used a set of 97 genes not involved in immune functions, to account for the lower effective population sizes in island species. We used synonymous and non-synonymous variations to estimate the selection pressure acting on immune genes. For the genes evolving under balancing selection, we used simulation to estimate the impact of population size variation. We found a significant effect of drift on immune genes of island species leading to a reduction in genetic diversity and efficacy of selection. However, the intensity of relaxed selection was not significantly different from control genes, except for MHC class II genes. These genes exhibit a significantly higher level of non-synonymous loss of polymorphism than expected assuming only drift and an evolution under frequency dependent selection, possibly due to a reduction of extracellular parasite communities on islands. Overall, our results showed that demographic effects lead to a decrease in the immune functions of island species, but the relaxed selection caused by a reduced parasite pressure may only occur in some immune genes categories.