Natural selection on MHC IIβ in parapatric lake and stream stickleback: Balancing, divergent, both or neither?

Abstract

Major histocompatibility complex (MHC) genes encode proteins that play a central role in vertebrates' adaptive immunity to parasites. MHC loci are among the most polymorphic in vertebrates' genomes, inspiring many studies to identify evolutionary processes driving MHC polymorphism within populations and divergence between populations. Leading hypotheses include balancing selection favouring rare alleles within populations, and spatially divergent selection. These hypotheses do not always produce diagnosably distinct predictions, causing many studies of MHC to yield inconsistent or ambiguous results. We suggest a novel strategy to distinguish balancing vs. divergent selection on MHC, taking advantage of natural admixture between parapatric populations. With divergent selection, individuals with immigrant alleles will be more infected and less fit because they are susceptible to novel parasites in their new habitat. With balancing selection, individuals with locally rare immigrant alleles will be more fit (less infected). We tested these contrasting predictions using three-spine stickleback from three replicate pairs of parapatric lake and stream habitats. We found numerous positive and negative associations between particular MHC IIβ alleles and particular parasite taxa. A few allele-parasite comparisons supported balancing selection, and others supported divergent selection between habitats. But, there was no overall tendency for fish with immigrant MHC alleles to be more or less heavily infected. Instead, locally rare MHC alleles (not necessarily immigrants) were associated with heavier infections. Our results illustrate the complex relationship between MHC IIβ allelic variation and spatially varying multispecies parasite communities: different hypotheses may be concurrently true for different allele-parasite combinations.

Gene expression stasis and plasticity following migration into a foreign environment

“…Both of these GO groups have known functions in parasite defence and have been previously implicated in the response to selection and parasite prevalence in stickleback (Bolnick & Stutz, ; Eizaguirre, Lenz, Kalbe, & Milinski, ; Lohman et al., In review). Previous studies revealed that Roberts Lake and Stream stickleback populations harbour significantly different parasite communities (Bolnick & Stutz, ), with corresponding differences in MHC Class II allele frequencies (Stutz & Bolnick, ).…”

“…MHC IIb was sequenced and data were analysed as described in Stutz and Bolnick (). A previous clinal survey of stickleback from this lake and stream revealed population differences in MHC IIb allele frequencies and significant associations between MHC alleles and the prevalence of particular parasites (Stutz & Bolnick, ). The lake–stream transplant experiment revealed that transplanted foreign fish accumulated higher parasite infections than native fish, but parasites apparently exploited native MHC genotypes (Bolnick & Stutz, ; Stutz & Bolnick, ).…”

“…However, lakes may be less predictable in other ways. For instance, lake stickleback consistently harbour more diverse parasite communities (Bolnick & Stutz, ; Stutz & Bolnick, ), and so may have evolved greater immunological plasticity to handle an unpredictable suite of pathogens and helminths.…”

“…We analyse data from a reciprocal transplant experiment using stickleback from Roberts Lake and Stream (Vancouver Island, British Columbia, Canada), whose fitness effects were previously reported by Bolnick and Stutz (). Prior studies have documented differences between these populations, with respect to genotype and phenotype (Weber, Bradburd et al., 2017; Stutz & Bolnick, ; Berner et al., , among others). Wild‐caught stickleback were trapped, weighed, measured for length, individually marked with unique spine clips and then placed in cylindrical wire cages.…”

“…We recently conducted a reciprocal transplant of threespine stickleback, moved between adjacent but ecologically very different lake and stream habitats (Bolnick & Stutz, ; Stuart et al., ). The lake and stream populations are divergent with respect to morphology (Berner, Grandchamp, & Hendry, ; Oke et al., ; Stuart et al., ), genomic SNPs (Weber, Bradburd, Stuart, Stutz, & Bolnick, 2017) and immune gene allele frequencies (MHC IIb, Stutz and Bolnick, ). These differences strongly suggest that there is divergent selection, yet our reciprocal transplant experiment yielded little signal of local adaptation (Bolnick & Stutz, ).…”