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

Major histocompatibility (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 favoring 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 versus 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 threespine 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, 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 multi-species parasite communities: different hypotheses may be concurrently true for different allele-parasite combinations.

主要组织相容性复合体（MHC）基因编码在脊椎动物抗寄生虫适应性免疫中发挥核心作用的蛋白质。MHC基因座是脊椎动物基因组中多态性最高的区域之一，诸多研究致力于阐明驱动种群内部MHC多态性及种群间分化的演化进程。主流假说包括青睐种群内部稀有等位基因的平衡选择，以及空间歧化选择。然而这些假说并非总能生成可明确区分的预测结果，导致诸多MHC相关研究的结论往往不一致或模糊不清。我们提出了一种全新策略，借助邻域种群间的自然基因渐渗，以区分MHC上的平衡选择与歧化选择：若存在空间歧化选择，携带外来等位基因的个体感染程度更高、适合度更低，因其对新栖息地中的新型寄生虫易感；若存在平衡选择，携带本地稀有外来等位基因的个体则具有更高的适合度（感染程度更低）。我们利用来自3对重复邻域湖泊与溪流生境的三刺棘鱼，对上述对立预测开展了验证。研究发现，特定MHC II类β链（MHC IIβ）等位基因与特定寄生虫类群之间存在大量正负相关关联。部分等位基因-寄生虫配对的结果支持平衡选择，其余则支持不同生境间的歧化选择。但整体而言，携带外来MHC等位基因的棘鱼并未表现出感染程度更高或更低的倾向。相反，本地稀有MHC等位基因（未必为外来等位基因）与更高的感染程度相关联。本研究结果揭示了MHC IIβ等位基因变异与空间异质性多物种寄生虫群落之间的复杂关联：不同假说可在不同的等位基因-寄生虫配对中同时成立。