Microbiome affects egg carotenoid investment, nestling development and adult oxidative costs of reproduction in Great tits

1. Parasites influence allocation trade-offs between reproduction and self-maintenance and consequently shape host life-history traits. The host microbiome includes pathogenic and commensal micro-organisms that are remarkable in their diversity and ubiquity. However, experimental studies investigating whether the microbiome shapes host reproduction are still lacking. 2. In this study, we tested whether the microbiome affects three important components of bird reproduction, namely (i) the maternal transfer of anti-microbial compounds to the eggs, (ii) the development of nestlings and (iii) the trade-off between reproduction and self-maintenance, here measured by the oxidative costs of reproduction. 3. We experimentally modified the microbiome of wild breeding Great tits (Parus major) by spraying nests with liquid solution that either favoured or inhibited bacterial growth compared to a control. These treatments modified the bacterial communities in the nests and on adult feathers. 4. We found that females from the treatment that decreased bacterial densities in the nests laid eggs with less carotenoids than females from the control, while we found no significant effect of increasing bacterial densities and modifying community composition compared to the control. Nestlings exposed to decreased bacterial densities grew faster and had longer tarsus length at fledging. Moreover, our analyses revealed that the relationship between investment in reproduction and oxidative damage was affected by the treatments. Adults raising larger clutches suffered higher oxidative damage in control nests, whereas this oxidative cost of reproduction was not detected when we modified bird microbiome. 5. Our study provides experimental evidence for an effect of the microbiome on egg carotenoid investment, nestling development and oxidative cost of reproduction and thus highlights the major effect that the microbiome may have on the evolution of host life-history strategies.

1. 寄生虫会影响宿主繁殖与自我维持之间的资源分配权衡，进而塑造宿主的生活史特征。宿主微生物组（microbiome）包含具有极高多样性与普遍性的致病性和共生微生物。然而，目前仍缺乏探究微生物组是否会塑造宿主繁殖能力的实验研究。
2. 本研究旨在验证微生物组是否会影响鸟类繁殖的三个关键维度：其一，母体向卵内传递抗微生物化合物的过程；其二，雏鸟的发育进程；其三，繁殖与自我维持之间的权衡（本研究通过繁殖的氧化成本对该权衡进行量化）。
3. 本研究通过向巢箱喷施特定液体溶液，对野生繁殖的大山雀（Great tit，学名*Parus major*）的微生物组进行实验调控：与对照组相比，该溶液可分别促进或抑制细菌生长。该调控手段成功改变了巢箱内以及成鸟羽毛表面的细菌群落结构。
4. 研究结果显示，相较于对照组，接受降低巢箱内细菌密度处理的雌鸟所产卵的类胡萝卜素（carotenoids）含量更低；而提高细菌密度并改变群落组成的处理未对产卵类胡萝卜素含量产生显著影响。暴露于低细菌密度环境的雏鸟生长速度更快，出飞时跗跖（tarsus）长度更长。此外，分析结果表明，繁殖投入与氧化损伤之间的关系受实验处理的调控：在对照组巢箱中，抚育更大窝卵数的成鸟会承受更高的氧化损伤，但在微生物组被调控的实验组中，未检测到该繁殖氧化成本。
5. 本研究为微生物组对鸟类卵内类胡萝卜素投入、雏鸟发育以及繁殖氧化成本的影响提供了实验证据，从而揭示了微生物组可能对宿主生活史策略的演化产生的重要作用。