What evolutionary processes maintain MHCIIβ diversity within and among
populations of stickleback?
Abstract
Major Histocompatibility Complex (MHC) genes encode for proteins that
recognize foreign protein antigens to initiate T-cell mediated adaptive
immune responses. They are often the most polymorphic genes in
vertebrate genomes. How evolution maintains this diversity is still an
unsettled issue. Three main hypotheses seek to explain the maintenance
of MHC diversity by invoking pathogen-mediated selection: heterozygote
advantage, frequency-dependent selection, and fluctuating selection
across landscapes or through time. Here, we use a large-scale field
parasite survey in a stickleback metapopulation to test predictions
derived from each of these hypotheses. We identify over a thousand
MHCIIβ alleles and find that many of them covary positively or
negatively with parasite load, suggesting that these genes contribute to
resistance or susceptibility. However, despite our large sample-size, we
find no evidence for the widely-cited stabilizing selection on MHC
heterozygosity, in which individuals with an intermediate number of MHC
alleles have the lowest parasite burden. Nor do we observe a rare-allele
advantage, or widespread fluctuating selection across populations. In
contrast, we find that MHC diversity is best predicted by neutral
genome-wide heterozygosity and between-population genomic divergence,
suggesting neutral processes are important in shaping the pattern of
metapopulation MHC diversity. Thus, although MHCIIβ is highly diverse
and relevant to the type and intensity of macroparasite infection in
these populations of stickleback, the main models of MHC evolution still
provide little explanatory power in this system.