Evolution of Copy Number at the MHC Varies across the Avian Tree of Life

Abstract

The evolution of the major histocompatibility complex (MHC) is shaped by frequent gene duplications and deletions, which generate extensive variation in the number of loci (gene copies) between different taxa. Here, we collected estimates of copy number at the MHC for over 250 bird species from 68 families. We found contrasting patterns of copy number evolution between MHC class I and class IIB, which encode receptors for intra- and extracellular pathogens, respectively. Across the avian evolutionary tree, there was evidence of accelerated evolution and stabilizing selection acting on copy number at class I, while copy number at class IIB was primarily influenced by fluctuating selection and drift. Reconstruction of MHC copy number variation showed ancestrally low numbers of MHC loci in nonpasserines and evolution toward larger numbers of loci in passerines. Different passerine lineages had the highest duplication rates for MHC class I (Sylvioidea) and class IIB (Muscicapoidea and Passeroidea). We also found support for the correlated evolution of MHC copy number and life-history traits such as lifespan and migratory behavior. These results suggest that MHC copy number evolution in birds has been driven by life histories and differences in exposure to intra- and extracellular pathogens.