Data from: A genetics-based approach confirms immune associations with life history across multiple populations of an aquatic vertebrate (Gasterosteus aculeatus)

Understanding how wild immune variation covaries with other traits can reveal how costs and trade-offs shape immune evolution in the wild. Divergent life history strategies may increase or alleviate immune costs, helping shape immune variation in a consistent, testable way. Contrasting hypotheses suggest that shorter life histories may alleviate costs by offsetting them against increased mortality; or increase the effect of costs if immune responses are traded off against development or reproduction. We investigated the evolutionary relationship between life history and immune responses within an island radiation of three-spined stickleback, with discrete populations of varying life histories and parasitism. We sampled two short-lived, two long-lived and an anadromous population using qPCR to quantify current immune profile and RAD-seq data to study the distribution of immune variants within our assay genes and across the genome. Short-lived populations exhibited significantly increased expression of all assay genes, which was accompanied by a strong association with population-level variation in local alleles and divergence in a gene that may be involved in complement pathways. In addition, divergence around the eda gene in anadromous fish is likely associated with increased inflammation. A wider analysis of 15 populations across the island revealed that immune genes across the genome show evidence of having diverged alongside life history strategies. Parasitism and reproductive investment were also important sources of variation for expression, highlighting the caution required when assaying immune responses in the wild. These results provide strong, gene-based support for current hypotheses linking life history and immune variation across multiple populations of a vertebrate model.

解析野生种群中免疫变异与其他性状的协同变化规律，可揭示免疫成本与权衡如何塑造自然界中的免疫演化进程。不同的生活史策略可能加剧或缓解免疫成本，以可被重复验证的一致方式塑造免疫变异格局。两种对立假说提出：短寿命生活史可通过将免疫成本与更高的死亡率相抵消来缓解成本；但若免疫应答需与发育或繁殖进行资源权衡，则会放大免疫成本的影响。本研究以岛屿辐射演化的三刺棘鱼（three-spined stickleback）为研究对象，该类群存在多个生活史与寄生压力各异的离散种群，旨在探究生活史与免疫应答间的演化关联。我们采集了2个短寿命种群、2个长寿命种群及1个溯河洄游种群（anadromous population），通过实时定量聚合酶链反应（qPCR）量化当前免疫表达谱，并借助限制性位点相关DNA测序（RAD-seq）分析靶标基因及全基因组范围内的免疫变异分布情况。短寿命种群的所有靶标基因表达量均显著上调，这与种群水平的本地等位基因变异及可能参与补体通路（complement pathways）的基因分化存在强关联。此外，溯河洄游鱼类中EDA基因（eda gene）周围区域的基因分化，可能与炎症水平升高相关。对该岛屿上15个种群的扩大范围分析显示，全基因组范围内的免疫基因均呈现出与生活史策略协同分化的信号。寄生压力与繁殖投入同样是基因表达变异的重要影响因素，这提示在野外开展免疫应答检测时需格外谨慎。本研究结果为脊椎动物模型类群中多个种群的生活史与免疫变异关联假说，提供了基于基因层面的强有力支持。