Among-lake reciprocal transplants induce convergent expression of immune genes in threespine stickleback

Geographic variation in parasite communities can drive evolutionary divergence in host immune genes. However, biotic and abiotic environmental variation can also induce plastic differences in immune function among populations. At present, there is little information concerning the relative magnitudes of heritable vs. induced immune divergence in natural populations. We examined immune gene expression profiles of threespine stickleback (Gasterosteus aculeatus) from six lakes on Vancouver Island, British Columbia. Parasite community composition differs between lake types (large or small, containing limnetic- or benthic-like stickleback) and between watersheds. We observed corresponding differences in immune gene expression profiles among wild-caught stickleback, using a set of seven immune genes representing distinct branches of the immune system. To evaluate the role of environmental effects on this differentiation, we experimentally transplanted wild-caught fish into cages in their native lake, or into a nearby foreign lake. Transplanted individuals' immune gene expression converged on patterns typical of their destination lake, deviating from their native expression profile. Transplant individuals' source population had a much smaller effect, suggesting relatively weak genetic underpinning of population differences in immunity, as viewed through gene expression. This strong environmental regulation of immune gene expression provides a counterpoint to the large emerging literature documenting microevolution and genetic diversification of immune function. Our findings illustrate the value of studying immunity in natural environmental settings where the immune system has evolved and actively functions.寄生虫群落的地理差异可驱动宿主免疫基因的进化分化。然而，生物与非生物环境变异同样可引发种群间免疫功能的表型可塑性差异。目前，关于自然种群中免疫分化的遗传基础与诱导性差异的相对强度，相关研究仍较为匮乏。我们对不列颠哥伦比亚省温哥华岛6处湖泊中的三刺鱼（threespine stickleback，*Gasterosteus aculeatus*）的免疫基因表达谱展开了研究。寄生虫群落组成在不同湖泊类型（即包含浮游型或底栖型三刺鱼的大、小型湖泊）以及不同流域间存在显著差异。我们通过一组涵盖免疫系统不同分支的7个免疫基因，发现野生捕获的三刺鱼的免疫基因表达谱存在相应差异。为评估环境效应对该表达分化的作用，我们将野生捕获的三刺鱼通过实验笼养的方式，分别移植至其原生湖泊或邻近的外来湖泊中。移植个体的免疫基因表达谱逐渐趋同于其迁入湖泊的典型模式，与它们原生种群的表达谱产生偏离。移植个体的源种群对表达谱的影响则相对微弱，这表明从基因表达层面来看，种群间免疫差异的遗传基础较为薄弱。这种对免疫基因表达的强烈环境调控，与近年来大量涌现的、记录免疫功能微进化与遗传分化的研究文献形成了有趣的对照。本研究结果表明，在免疫系统进化并持续发挥功能的自然环境中开展免疫研究具有重要价值。