Divergent sex-specific effects of an IgE receptor polymorphism: from immunity to health, and ultimately, fitness

Abstract

AbstractThe genotype of an individual is an important predictor of their immune function, and subsequently, their ability to stay fit and healthy. However, the same genotype, subjected to different environments, can also result in divergent outcomes. The sexes represent two such different environments. Sexual dimorphism is widespread across the animal kingdom. Despite this, very little is known about the importance of sex for the expression of genotype in the context of health and disease, particularly in natural populations. We combined data on genotype, immune gene expression, infection incidence and pedigree of individuals in a natural population of field voles (Microtus agrestis). We identified a polymorphism in the high-affinity Immunoglobulin E (IgE) receptor (GC and non-GC haplotypes) that has divergent effects on the immunity, health and fitness of males and females. The GC haplotype was associated with increases in the expression of both pro- and anti-inflammatory genes regardless of sex. However, we found that the signal was stronger for pro-inflammatory genes in males with the GC haplotype, who also had the same risk of infection and a lower reproductive success when compared to males with non-GC haplotypes. In contrast, females with the GC haplotype showed a stronger signal for anti-inflammatory genes, a higher risk of infection and the same reproductive success when compared to females with non-GC haplotypes. To our knowledge, this is the first time that a polymorphism with divergent sex-specific effects across all three levels (immunity, health and fitness) has been documented in a natural population.