Bacterial dispersal and drift drive microbiome diversity patterns within a population of feral hindgut fermenters

Studies of microbiome variation in wildlife often emphasize host
physiology and diet as proximate selective pressures acting on
host-associated microbiota. In contrast, microbial dispersal and
ecological drift are more rarely considered. Using amplicon sequencing, we
characterized the bacterial microbiome of adult female (n = 86) Sable
Island horses (Nova Scotia, Canada) as part of a detailed individual-based
study of this feral population. Using data on sampling date, horse
location, age, parental status, and local habitat variables, we contrasted
the ability of spatiotemporal, life history, and environmental factors to
explain microbiome diversity among Sable Island horses. We extended
inferences made from these analyses with both phylogeny-informed and
phylogeny-independent null modeling approaches to identify deviations from
stochastic expectations. Phylogeny-informed diversity measures were
correlated with spatial and local habitat variables, but null modelling
results suggested that heterogeneity in ecological drift, rather than
differential selective pressures acting on the microbiome, was responsible
for these correlations. Conversely, phylogeny-independent diversity
measures were best explained by host spatial and social structure,
suggesting that taxonomic composition of the microbiome was shaped most
strongly by bacterial dispersal. Parental status was important but
correlated with measures of β-dispersion rather than β-diversity (mares
without foals had lower alpha diversity and more variable microbiomes than
mares with foals). Our results suggest that between host microbiome
variation within the Sable Island horse population is driven more strongly
by bacterial dispersal and ecological drift than by differential selective
pressures. These results emphasize the need to consider alternative
ecological processes in the study of microbiomes.

针对野生动物微生物组（microbiome）变异的相关研究，通常将宿主生理学与饮食视作作用于宿主相关微生物组的直接选择压力。与之形成鲜明对比的是，微生物扩散与生态漂变这两类过程却较少得到关注。本研究以加拿大新斯科舍省赛博岛野马这一已开展细致个体追踪的野生种群为研究对象，通过扩增子测序（amplicon sequencing）技术，对86只成年雌性赛博岛野马的细菌微生物组进行了表征。我们收集了采样日期、马匹位置、年龄、母马育幼状态以及局部生境变量等多维度数据，对比了时空因素、生活史特征与环境因子对赛博岛野马微生物组多样性的解释能力。同时，我们分别采用系统发育关联（phylogeny-informed）与非系统发育关联（phylogeny-independent）的空模型（null modeling）分析方法，拓展了上述分析的推论效力，以识别偏离随机预期的群落模式。系统发育关联的多样性指标与空间及局部生境变量呈显著相关，但空模型分析结果显示，此类相关性源于生态漂变的异质性，而非微生物组所受的差异化选择压力。反之，非系统发育关联的多样性指标则可通过宿主的空间分布与社会结构得到最佳解释，提示微生物组的分类组成主要受细菌扩散过程塑造。母马育幼状态对微生物组亦存在显著影响，但其效应与β离散度（β-dispersion）相关，而非β多样性（beta diversity）：与育有幼驹的母马相比，无幼驹母马的α多样性（alpha diversity）更低，且微生物组变异程度更高。本研究结果表明，赛博岛野马种群内宿主间的微生物组差异，主要由细菌扩散与生态漂变驱动，而非差异化的选择压力。上述研究结果强调，在微生物组研究领域，需同时考虑其他潜在的生态过程。