Data from: Experimental evolution of insect immune memory versus pathogen resistance

Under strong pathogen pressure, insects often evolve resistance to infection. Many insects are also protected via immune memory (‘immune priming’), whereby sub-lethal exposure to a pathogen enhances survival after secondary infection. Theory predicts that immune memory should evolve when the pathogen is highly virulent, or when pathogen exposure is relatively rare. However, there are no empirical tests of these hypotheses, and the adaptive benefits of immune memory relative to direct resistance against a pathogen are poorly understood. To determine the selective pressures and ecological conditions that shape immune evolution, we imposed strong pathogen selection on flour beetle (Tribolium castaneum) populations, infecting them with Bacillus thuringiensis (Bt) for 11 generations. Populations injected first with heat-killed and then live Bt each generation evolved high basal resistance against multiple Bt strains. In contrast, populations injected only with a high dose of live Bt evolved a less effective but strain-specific priming response. Control populations injected with heat-killed Bt did not evolve priming; and in the ancestor, priming was effective only against a low Bt dose. Intriguingly, one replicate population first evolved priming and subsequently evolved basal resistance, suggesting the potential for dynamic evolution of different immune strategies. Our work is the first report showing that pathogens can select for rapid modulation of insect priming ability, allowing hosts to evolve divergent immune strategies (generalized resistance vs. specific immune memory) with potentially distinct mechanisms.

在强病原体选择压力下，昆虫通常会演化出针对感染的抗性。许多昆虫还可通过免疫记忆（immune priming）获得保护：即经亚致死剂量的病原体暴露后，宿主在二次感染中的存活率会得到提升。理论预测，当病原体毒力极强或病原体暴露频率相对较低时，免疫记忆应当会发生演化。然而，目前尚无针对这些假说的实证检验，且人们对免疫记忆相较于直接抗病原体感染的适应性优势仍知之甚少。为明确塑造免疫系统演化的选择压力与生态条件，我们对赤拟谷盗（Tribolium castaneum）种群施加了强病原体选择压力，采用苏云金芽孢杆菌（Bacillus thuringiensis, Bt）连续11代感染其种群。每代先经热灭活Bt再经活Bt接种的种群，演化出了对多种Bt菌株的高水平基础抗性。与之相对，仅接种高剂量活Bt的种群则演化出了效果较弱但具备菌株特异性的致敏应答。接种热灭活Bt的对照组种群未出现致敏现象；且在原始祖先种群中，致敏应答仅对低剂量Bt有效。值得注意的是，有一个重复种群先演化出致敏应答，随后又演化出基础抗性，这提示不同免疫策略可能存在动态演化的潜力。本研究首次报道了病原体可通过选择作用快速调控昆虫的免疫致敏能力，使宿主得以演化出两种差异化的免疫策略——广谱抗性与特异性免疫记忆，且二者可能具备不同的作用机制。