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

Abstract

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.

A global analysis of selection at the avian MHC

“…This may be especially relevant for MHC because strong balancing selection can maintain alleles for long evolutionary times, often beyond species divergence (Cutrera and Lacey ; Minias et al. ). In fact, within our dataset we found several cases of MHC alleles shared between avian genera, which are estimated to have diverged 20–30 million years ago (Supporting Information .…”

“…Since MHC alleles can be maintained for long evolutionary times, the historical signature of recombination can be retained beyond species divergence (Minias et al. ) and, thus, we assessed recombination at the inter‐specific level (Supporting Information . All recombinant sequences were removed from the alignments and FUBAR models were re‐run for passerine and non‐passerine datasets.…”

Polymorphism at expressed DQ and DR loci in five common equine MHC haplotypes

“…Gene conversion is a mechanism whereby novel polymorphism is created in a recipient gene from a template of nucleotides originating in a donor gene (Hogstrand and Bohme, 1999). Gene conversion events have been reported in MHC class II loci of the pig (Brunsberg et al, 1996) and sheep (Hickford et al, 2004), and a recent study in grouse reports a significant role for gene conversion in maintaining diversity in the Class II region of that species (Minias et al, 2016). …”

Specific alleles at immune genes, rather than genome‐wide heterozygosity, are related to immunity and survival in the critically endangered Attwater's prairie‐chicken

“…; Minias et al . ), we expected to amplify a maximum of two (class I) and four (class II) alleles within individuals.…”

“…To amplify MHC class II (exon 2), we used primers Blex2F (Eimes et al 2010) and RNA R1a (Strand et al 2007) to amplify a 239-bp fragment (for PCR conditions see, Eimes et al 2010). Prairie-chickens have a single class I locus and two class II loci (Eimes et al 2013), and similar to our previous work in prairie grouse (Bateson et al 2015;Minias et al 2016), we expected to amplify a maximum of two (class I) and four (class II) alleles within individuals.…”