Trade-offs in expressed major histocompatibility complex diversity seen on a macroevolutionary scale among songbirds

Abstract

To survive organisms must defend themselves against pathogens. Classical Major Histocompatibility Complex (MHC) genes play a key role in pathogen defense by encoding molecules involved in pathogen recognition. MHC gene diversity influences the variety of pathogens individuals can recognize and respond to and has consequently been a popular genetic marker for disease resistance in ecology and evolution. However, MHC diversity is predominantly estimated using genomic DNA (gDNA) with little knowledge of expressed diversity. This limits our ability to interpret the adaptive significance of variation in MHC diversity, especially in species with very many MHC genes such as songbirds. Here, we address this issue using phylogenetic comparative analyses of the number of MHC class I alleles (MHC-I diversity) in gDNA and complementary DNA (cDNA), that is, expressed alleles, across 13 songbird species. We propose three theoretical relationships that could be expected between genomic and expressed MHC-I diversity on a macroevolutionary scale and test which of these are best supported. In doing so, we show that significantly fewer MHC-I alleles than the number available are expressed, suggesting that optimal MHC-I diversity could be achieved by modulating gene expression. Understanding the relationship between genomic and expressed MHC diversity is essential for interpreting variation in MHC diversity in an evolutionary context.

Keywords: Birds; Gene expression; MHC diversity; MHC genes; Major Histocompatibility Complex.