Contrasting evolutionary histories of MHC class I and class II loci in grouse--effects of selection and gene conversion.

Genes of the major histocompatibility complex (MHC) encode receptor molecules that are responsible for recognition of intracellular and extracellular pathogens (class I and class II genes, respectively) in vertebrates. Given the different roles of class I and II MHC genes, one might expect the strength of selection to differ between these two classes. Different selective pressures may also promote different rates of gene conversion at each class. Despite these predictions, surprisingly few studies have looked at differences between class I and II genes in terms of both selection and gene conversion. Here, we investigated the molecular evolution of MHC class I and II genes in five closely related species of prairie grouse (Centrocercus and Tympanuchus) that possess one class I and two class II loci. We found striking differences in the strength of balancing selection acting on MHC class I versus class II genes. More than half of the putative antigen-binding sites (ABS) of class II were under positive or episodic diversifying selection, compared with only 10% at class I. We also found that gene conversion had a stronger role in shaping the evolution of MHC class II than class I. Overall, the combination of strong positive (balancing) selection and frequent gene conversion has maintained higher diversity of MHC class II than class I in prairie grouse. This is one of the first studies clearly demonstrating that macroevolutionary mechanisms can act differently on genes involved in the immune response against intracellular and extracellular pathogens.

Greater prairie chickens have a compact MHC-B with a single class IA locus.

The major histocompatibility complex (MHC) plays a central role in innate and adaptive immunity, but relatively little is known about the evolution of the number and arrangement of MHC genes in birds. Insights into the evolution of the MHC in birds can be gained by comparing the genetic architecture of the MHC between closely related species. We used a fosmid DNA library to sequence a 60.9-kb region of the MHC of the greater prairie chicken (Tympanuchus cupido), one of five species of Galliformes with a physically mapped MHC. Greater prairie chickens have the smallest core MHC yet observed in any bird species, and major changes are observed in the number and arrangement of MHC loci. In particular, the greater prairie chicken differs from other Galliformes in the deletion of an important class I antigen binding gene. Analysis of the remaining class IA gene in a population of greater prairie chickens in Wisconsin, USA revealed little evidence for selection at the region responsible for antigen binding.