Abstract
A distinguishing characteristic of genes that code for the major histocompatibility complex (MHC) is that alleles often share more similarity between, rather than within species. There are two likely mechanisms that can explain this pattern: convergent evolution and trans-species polymorphism (TSP), in which ancient allelic lineages are maintained by balancing selection and retained by descendant species. Distinguishing between these two mechanisms has major implications in how we view adaptation of immune genes. In this study we analyzed exon 2 of the MHC class IIB in three passerine bird species in the genus Corvus: jungle crows (Corvus macrorhynchos japonensis) American crows (C. brachyrhynchos) and carrion crows (C. corone orientalis). Carrion crows and American crows are recently diverged, but allopatric, sister species, whereas carrion crows and jungle crows are more distantly related but sympatric species, and possibly share pathogens linked to MHC IIB polymorphisms. These patterns of evolutionary divergence and current geographic ranges enabled us to test for trans-species polymorphism and convergent evolution of the MHC IIB in crows. Phylogenetic reconstructions of MHC IIB sequences revealed several well supported interspecific clusters containing all three species, and there was no biased clustering of variants among the sympatric carrion crows and jungle crows. The topologies of phylogenetic trees constructed from putatively selected sites were remarkably different than those constructed from putatively neutral sites. In addition, trees constructed using non-synonymous substitutions from a continuous fragment of exon 2 had more, and generally more inclusive, supported interspecific MHC IIB variant clusters than those constructed from the same fragment using synonymous substitutions. These phylogenetic patterns suggest that recombination, especially gene conversion, has partially erased the signal of allelic ancestry in these species. While clustering of positively selected amino acids by supertyping revealed a single supertype shared by only jungle and carrion crows, a pattern consistent with convergence, the overall phylogenetic patterns we observed suggest that TSP, rather than convergence, explains the interspecific allelic similarity of MHC IIB genes in these species of crows.
Highlights
The major histocompatibility complex (MHC) is an unusual example of a functional gene complex that exhibits high levels of polymorphism
If this study been limited to the sympatric carrion crows and jungle crows, we may have erroneously concluded that convergent evolution explains these patterns; inclusion of sequences from the allopatric American crow, and the resulting interspecific clustering of all three species at functional sites, suggests that the pattern observed in the phylogenies is not convergence, but rather trans-species polymorphism
Our results indicate that the MHC IIB in crows exhibits the same characteristics of the MHC IIB observed in other passerine species (Bollmer et al, 2010; Zagalska-Neubauer et al, 2010), namely, high levels of polymorphism, highly duplicated loci, probable copy number variation of loci and a strong signature of selection
Summary
The major histocompatibility complex (MHC) is an unusual example of a functional gene complex that exhibits high levels of polymorphism. The MHC is the most polymorphic coding gene family in vertebrate genomes (Klein, 1986) and the maintenance of this polymorphism is usually attributed to pathogen-mediated balancing selection (Sommer, 2005), sexual selection, as well as molecular mechanisms such as recombination and gene conversion, may play important roles (Andersson & Mikko, 1995; Martinsohn et al, 1999; Zelano & Edwards, 2002). One distinguishing characteristic of MHC genes is that alleles often share more similarity between rather than among species. Two mechanisms have been proposed to explain this “trans-specific” similarity of MHC alleles. The first explanation, called “trans-species polymorphism” (TSP), proposes that orthologous MHC allelic lineages are maintained by balancing selection, often over macro-evolutionary time-scales, and persist through speciation events (Klein et al, 1998). Strong evidence for TSP in MHC IIB genes has been found in a wide range of taxa, those of mammals and fish (Klein et al, 1993; Graser et al, 1996; Garrigan & Hedrick, 2003; Lenz et al, 2013)
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