Worsley Sarah F, Lee Chuen Zhang, Versteegh Maaike A, Burke Terry, Komdeur Jan, Dugdale Hannah L, Richardson David S
School of Biological Sciences, University of East Anglia, Norwich Research Park, Norfolk NR4 7TJ, United Kingdom.
Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, P.O. Box 11103, 9700 CC, Groningen, The Netherlands.
ISME Commun. 2025 Aug 11;5(1):ycaf138. doi: 10.1093/ismeco/ycaf138. eCollection 2025 Jan.
Environmental variation is a key factor shaping microbial communities in wild animals. However, most studies have focussed on separate populations distributed over large spatial scales. How ecological factors shape inter-individual microbiome variation within a single landscape and host population remains poorly understood. Here, we use dense sampling of individuals in a natural, closed population of Seychelles warblers () on Cousin Island (<0.7 km diameter, 0.34 km total area) to determine whether gut microbiome communities exhibit high-resolution spatial variation over fine scales (average territory area is 0.0023 km). We identified a small but highly significant quadratic relationship between geographic distance and gut microbiome beta diversity across the island. Microbiome composition initially diverged with increasing geographic distance between territories. However, after ca. >300 m, microbiome composition became increasingly similar amongst individuals situated on different sides of the island. This relationship was robust to the effects of host relatedness, age, and sex. Further analysis showed that microbiome composition differed between individuals inhabiting coastal and inland territories. Warblers in coastal territories harboured greater abundances of marine bacteria and lower abundances of anaerobic taxa commonly linked to host metabolic health, suggesting that exposure to different environmental microbes and variation in host condition (which is lower in coastal territories) could drive spatial patterns of gut microbiome variation across the island. This work demonstrates that host-microbe interactions can be labile even at very fine spatial scales. Such variability may have implications for how species respond to anthropogenic disturbance in wild habitats.
环境变化是塑造野生动物微生物群落的关键因素。然而，大多数研究都集中在分布于大空间尺度上的不同种群。生态因素如何在单一景观和宿主种群中塑造个体间微生物组的差异仍知之甚少。在此，我们对 Cousin 岛（直径<0.7 千米，总面积 0.34 平方千米）上自然封闭的塞舌尔莺种群进行密集个体采样，以确定肠道微生物群落是否在精细尺度上呈现高分辨率的空间变异（平均领地面积为 0.0023 平方千米）。我们发现全岛地理距离与肠道微生物组β多样性之间存在微小但高度显著的二次关系。微生物组组成最初随着领地间地理距离的增加而分化。然而，在大约>300 米之后，位于岛屿不同侧的个体之间的微生物组组成变得越来越相似。这种关系对宿主亲缘关系、年龄和性别的影响具有稳健性。进一步分析表明，栖息在沿海和内陆领地的个体之间微生物组组成存在差异。沿海领地的莺类体内海洋细菌丰度更高，而与宿主代谢健康通常相关的厌氧类群丰度更低，这表明接触不同的环境微生物以及宿主状况的差异（沿海领地的宿主状况较低）可能驱动全岛肠道微生物组变异的空间模式。这项工作表明，即使在非常精细的空间尺度上，宿主 - 微生物相互作用也可能不稳定。这种变异性可能对物种如何应对野生栖息地的人为干扰产生影响。
