National Centre for Biological Sciences, Tata Institute of Fundamental Research, GKVK, Bangalore, India.
Ashoka University, Sonepat, Rai, India.
J Anim Ecol. 2019 Sep;88(9):1332-1342. doi: 10.1111/1365-2656.13030. Epub 2019 Jun 14.
In many insects, individuals primed with low doses of pathogens early in life have higher survival after exposure to the same pathogen later in life. Yet, our understanding of the evolutionary and ecological history of priming of immune response in natural insect populations is limited. Previous work demonstrated population-, sex- and stage-specific variation in the survival benefit of priming response in flour beetles (Tribolium castaneum) infected with their natural pathogen Bacillus thuringiensis. However, the evolutionary forces responsible for this natural variation remained unclear. In the present work, we tested whether the strength of the priming response (measured as the survival benefit after priming and subsequent infection, relative to unprimed controls) was associated with multiple fitness parameters and immune components across 10 flour beetle populations collected from different locations in India. Our results suggest two major selective pressures that may explain the observed inter-population variation in priming: (a) Basal pathogen susceptibility - populations that were more susceptible to infection produced a stronger priming response, and (b) Short-term early reproductive success - populations where primed females produced more offspring early in life (measured over 2 days) had lower survival benefit (measured over 120 days), suggesting a potential trade-off between early reproduction and priming response. However, the negative association between survival and reproduction is limited to priming and infection in adults, but not in larvae. While other components of beetle fitness (starvation resistance and larval development) and immune function (haemolymph antibacterial activity and antimicrobial quinone secretion) also varied widely across populations, none of them was correlated with the variation in priming responses across populations. Our work is the first systematic empirical demonstration of multiple selective pressures that may govern the evolution of immune priming in the wild. We hope that this motivates further experiments to establish the role of pathogen-imposed selection and fitness costs in the evolution of priming in natural insect populations.
在许多昆虫中，个体在生命早期接触低剂量病原体后，在以后的生活中暴露于相同的病原体后，其存活率更高。然而，我们对自然昆虫种群中免疫反应引发的进化和生态历史的理解是有限的。以前的工作表明，在感染其天然病原体苏云金芽孢杆菌的粉斑螟（Tribolium castaneum）中，种群、性别和阶段特异性的免疫反应引发的生存效益存在差异。然而，导致这种自然变异的进化力量尚不清楚。在本研究中，我们测试了引发反应的强度（通过引发和随后的感染后的生存效益来衡量，相对于未引发的对照）是否与印度不同地点采集的 10 个粉斑螟种群的多个适应度参数和免疫成分相关。我们的结果表明，有两个主要的选择压力可以解释所观察到的引发反应的种群间变异：（a）基础病原体易感性 - 对感染更敏感的种群产生更强的引发反应，（b）短期早期繁殖成功 - 引发的雌性在生命早期（测量 2 天）产生更多后代的种群，其生存效益（测量 120 天）较低，表明早期繁殖和引发反应之间可能存在潜在的权衡。然而，生存和繁殖之间的负相关仅限于成虫的引发和感染，但幼虫则不然。虽然甲虫适应度的其他组成部分（饥饿抵抗和幼虫发育）和免疫功能（血淋巴抗菌活性和抗菌醌分泌）在种群之间也有很大差异，但它们都与种群之间引发反应的变化无关。我们的工作是第一个系统地实证证明了多种选择压力可能控制了野生免疫引发的进化。我们希望这将进一步激发实验，以确定病原体施加的选择和适应成本在自然昆虫种群中引发进化的作用。
