Gut microbes shape many aspects of organismal biology, yet how these key bacteria transmit among hosts in natural populations remains poorly understood. Recent work in mammals has emphasized either transmission through social contacts or indirect transmission through environmental contact, but the relative importance of different routes has not been directly assessed. Here we used a novel radio-frequency identification-based tracking system to collect long-term high-resolution data on social relationships, space use and microhabitat in a wild population of mice (Apodemus sylvaticus), while regularly characterizing their gut microbiota with 16S ribosomal RNA profiling. Through probabilistic modelling of the resulting data, we identify positive and statistically distinct signals of social and environmental transmission, captured by social networks and overlap in home ranges, respectively. Strikingly, microorganisms with distinct biological attributes drove these different transmission signals. While the social network effect on microbiota was driven by anaerobic bacteria, the effect of shared space was most influenced by aerotolerant spore-forming bacteria. These findings support the prediction that social contact is important for the transfer of microorganisms with low oxygen tolerance, while those that can tolerate oxygen or form spores may be able to transmit indirectly through the environment. Overall, these results suggest social and environmental transmission routes can spread biologically distinct members of the mammalian gut microbiota.

肠道微生物塑造了生物体生物学的许多方面，但这些关键细菌如何在自然群体的宿主之间传播仍然知之甚少。最近在哺乳动物中的研究强调通过社会接触传播或通过环境接触间接传播，但不同途径的相对重要性尚未得到直接评估。在这里，我们使用一种新型的基于射频识别的跟踪系统来收集野生小鼠（ Apodemus sylvaticus ）的社会关系、空间利用和微栖息地的长期高分辨率数据，同时定期使用 16S 核糖体来表征它们的肠道微生物群RNA 分析。通过对结果数据进行概率建模，我们分别识别了社交网络和家庭范围重叠捕获的社会和环境传播的积极且统计上不同的信号。引人注目的是，具有不同生物属性的微生物驱动了这些不同的传输信号。虽然社交网络对微生物群的影响是由厌氧细菌驱动的，但共享空间的影响最大的是耐氧孢子形成细菌的影响。这些发现支持这样的预测：社会接触对于低氧耐受性微生物的传播很重要，而那些能够耐受氧或形成孢子的微生物可能能够通过环境间接传播。总的来说，这些结果表明社会和环境传播途径可以传播哺乳动物肠道微生物群中生物学上不同的成员。