Pig microbial and immune traits respond to host evolutionary history and ecology across multiple scales (metagenomics). pig gut metagenome

Animal ecology and evolution has long been known to shape host physiology, but more recently, the gut microbiome has been identified as a mediator between host ecology and evolution and host health. Gut microbiome responses to new animal genotypes and local environmental change during domestication may be linked to the appearance of specific host phenotypes that are adaptive (or not) to the domestic environment. Because ensuring the wellbeing of domestic animals is of the utmost importance for the agricultural sector, the influence of the gut microbiome on immune homeostasis and metabolism are particularly critical to understand. We investigated how domestication affects the gut microbiome and host immune state in multiple populations of free-ranging feral pigs, captive wild pigs, and free-ranging and captive domestic pigs. We observed that pig evolutionary history contributed to the repertoire of metabolic genes found in the gut microbiome, whereas domestication context explained the most variation in microbiome composition, pathogen and antibiotic resistance gene (ARG) abundances, and immune markers. We also documented population-level effects within domestication contexts, demonstrating that fine scale environmental variation also shaped host and microbe features. Our findings highlight that understanding which gut microbiome and immune traits respond to either host evolutionary history and/or local ecology will inform targeted interventions that manipulate the gut microbiome to achieve beneficial health outcomes.

长期以来，学界已知动物生态学与进化过程会塑造宿主生理机能；而近年来的研究进一步证实，肠道微生物组（gut microbiome）是连接宿主生态学、进化与宿主健康的关键介导因子。在动物驯化过程中，肠道微生物组对宿主新基因型与局域环境变化的响应，或与宿主特定表型的出现密切相关——这类表型对驯化环境或具备适应性，或无适应性。鉴于保障家畜健康对农业产业具有至关重要的意义，解析肠道微生物组对免疫稳态（immune homeostasis）与代谢的调控作用，便显得尤为关键。本研究针对多组群的自由放养野化猪、圈养野生野猪，以及自由放养与圈养家猪开展实验，探究驯化过程如何影响肠道微生物组与宿主免疫状态。研究结果显示，猪的进化历史决定了肠道微生物组中代谢基因的组成谱系；而驯化背景则是解释微生物组组成、病原体与抗生素抗性基因（antibiotic resistance gene, ARG）丰度，以及免疫标志物变异的最主要因素。本研究同时记录了驯化背景下的种群水平效应，证实细尺度环境变异同样会塑造宿主与微生物的相关特征。本研究结果表明，明确哪些肠道微生物组与免疫性状会响应宿主进化历史或局域生态环境，将为通过调控肠道微生物组以实现有益健康目标的精准干预手段提供理论指导。