Genes of the major histocompatibility complex (MHC) encode antigen binding molecules and are an integral part of the acquired immune response of vertebrates. In general, high individual MHC diversity is expected to increase fitness by broadening the spectrum of pathogens recognized by the immune system, in accordance with the heterozygote advantage mechanism. On the other hand, the optimality hypothesis assumes that individuals with optimal (intermediate), rather than maximum diversity of the MHC will achieve the highest fitness because of inherent costs associated with expressing diverse MHC alleles.

Here, we tested for associations between individual diversity of the MHC class I and class II genes (binding antigens of intra- and extra-cellular pathogens, respectively) and a range of fitness-related traits (condition, ornament expression and reproduction) in an urban population of the Eurasian coot Fulica atra.

Contrary to our expectation, we found that high within-individual allelic diversity of MHC genes (both class I and II) was associated with poorer condition (lower blood haemoglobin concentrations), weaker expression of the putative ornament (smaller frontal shield), later onset of breeding and smaller clutches. An analysis of functional MHC allele clusters (supertypes) provided further support for negative associations of MHC diversity with phenotypic quality and reproductive performance, but most of these relationships could not be explained by the presence of specific maladaptive supertypes. Finally, we found little empirical support for the optimality hypothesis in the Eurasian coot.

Our results suggest that the costs of high MHC diversity outweighed any benefits associated with broad MHC repertoire, which could be driven by depauperate pathogen diversity in an urban landscape. To the best of our knowledge, this is one of the first studies providing consistent evidence for negative associations of MHC diversity with a range of fitness-related traits in a natural avian population.