Food supplementation affects gut microbiota and immunological resistance to parasites in a wild bird species

<b>Abstract</b>1. Supplemental feeding can increase the overall health of animals but also can have varying consequences for animals dealing with parasites. Furthermore, the mechanism mediating the effect of food supplementation on host-parasite interactions remains poorly understood.2. The goal of the study was to determine the effect of food supplementation on host defenses against parasitic nest flies and whether host gut microbiota, which can affect immunity, potentially mediates these relationships. In a fully crossed design, I experimentally manipulated the abundance of parasitic nest flies (<i>Protocalliphora sialia</i>) and food availability then characterized the gut microbiota, immune responses, and nest parasite abundance of nestling eastern bluebirds (<i>Sialia sialis</i>).3. Food supplemented birds had 75% fewer parasites than unsupplemented birds. Parasite abundance decreased throughout the breeding season for unsupplemented birds, but abundance did not change throughout the season for supplemented birds. Food supplementation increased overall fledging success. Parasitism had a sublethal effects on blood loss, but food supplementation mitigated these effects by increasing parasite resistance via the nestling IgY antibody response.4. Food supplementation increased the gut bacterial diversity in nestlings, which was negatively related to parasite abundance. Food supplementation also increased the relative abundance of <i>Clostridium</i>spp. in nestlings, which was positively related to their antibody response and negatively related to parasite abundance. 5. <i>Synthesis and applications</i>. Overall, these results suggest that food supplementation, especially early in the breeding season, increases resistance to parasitism during the early life stage of the host, which could be mediated by the effect of supplementation on the gut microbiota. Wildlife food supplementation is a common pastime for humans worldwide and therefore it is important to determine the consequences of this activity on animal health. Furthermore, supplemental feeding could induce resistance to detrimental parasites (e.g. invasive parasites) in hosts when management of the parasite is not immediately possible.

**摘要**1. 补充饲喂（supplemental feeding）可提升动物整体健康水平，但同时对感染寄生虫的动物会产生各异的影响。此外，介导食物补充对宿主-寄生虫互作（host-parasite interactions）影响的具体机制仍尚未明确。2. 本研究旨在明确补充饲喂对宿主抵御寄生性巢蝇的作用，以及可影响宿主免疫的肠道微生物群（gut microbiota）是否会潜在调控这一关联。本研究采用完全交叉实验设计，通过人工操控寄生性巢蝇（*Protocalliphora sialia*）的种群丰度与食物可获得性，对东蓝鸲（*Sialia sialis*）雏鸟的肠道微生物群、免疫反应以及巢内寄生虫丰度进行了表征分析。3. 接受补充饲喂的雏鸟，其寄生虫感染量较未饲喂组低75%。未饲喂组雏鸟的寄生虫丰度随繁殖季推进逐渐降低，而饲喂组的寄生虫丰度则无显著季节变化。补充饲喂可提升整体离巢成功率。寄生虫感染会对雏鸟造成亚致死性失血，但补充饲喂可通过增强雏鸟的IgY抗体（IgY antibody）反应提升抗寄生虫能力，从而缓解该不良影响。4. 补充饲喂可提升雏鸟的肠道细菌多样性，而该多样性与寄生虫丰度呈负相关。此外，补充饲喂还可提升雏鸟体内梭菌属（Clostridium）的相对丰度，该相对丰度与雏鸟的抗体反应呈正相关，与寄生虫丰度呈负相关。5. **综合与应用**。整体而言，本研究结果表明，补充饲喂（尤其是在繁殖季早期）可提升宿主早期生活阶段的抗寄生虫能力，这一效应可能通过饲喂对肠道微生物群的调控作用实现。全球范围内，野生动物补充饲喂是一项常见的人类活动，因此明确该活动对动物健康的影响至关重要。此外，在无法立即开展寄生虫防治工作时，补充饲喂可诱导宿主对有害寄生虫（如入侵性寄生虫）产生抗性。