Wolves & the MHC: variability, hybridization and mate choice in the Italian wolf population

Isolated small populations may experience low adaptability and increased extinction risks due to reduced genetic variability, especially if at important functional genes such as the Major Histocompatibility Complex (MHC). We investigated the variability of three class-II genes (DRB1, DQA1, DQB1) in the Italian wolf population, which was long isolated and is now expanding after a recent bottleneck. Compared to other populations, we still found a remarkable MHC variability, showing signatures of historical selection (high dN/dS ratio). The Italian wolves are known to hybridize with domestic dogs, and dog-derived MHC alleles were detected in some genetically-admixed individuals. Background microsatellite and MHC loci did not show reduced variability due to the recent bottleneck. Thus, the population recovery seems not to be threatened by reduced MHC variation nor by deep introgression of domestic dog alleles. The observed variability could be also influenced by reproductive patterns, which can rely upon MHC similarity between mates. Based on pedigree data of wild-living packs, as reconstructed from extensive non-invasive genetic sampling, we tested the hypothesis of non-random mate choice in 26 breeding pairs. Results showed an unexpected prevalence of MHC-based assortative mating, with excess of peptide similarity between breeding pair members as compared to random expectations. Moreover, variation in both relatedness and heterozygosity showed significant positive correlations with fitness traits (total offspring, years as reproducers, mean offspring per year) deduced from pedigrees. These findings suggest possible advantages for breeders that are more related at the MHC, but not at the genetic background. This balance of general inbreeding avoidance, MHC-assortative mating and heterozygote advantage can reflect the social structure of the species, potentially maximizing the adaptation to the environmental pressures.