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Specialized host–microbe symbioses canonically show greater diversity than expected from simple models, both at the population level and within individual hosts. To understand how this heterogeneity arises, we utilize the squash bug, Anasa tristis , and its bacterial symbionts in the genus Caballeronia . We modulate symbiont bottleneck size and inoculum composition during colonization to demonstrate the significance of ecological drift, the noisy fluctuations in community composition due to demographic stochasticity. Consistent with predictions from the neutral theory of biodiversity, we found that ecological drift alone can account for heterogeneity in symbiont community composition between hosts, even when 2 strains are nearly genetically identical. When acting on competing strains, ecological drift can maintain symbiont genetic diversity among different hosts by stochastically determining the dominant strain within each host. Finally, ecological drift mediates heterogeneity in isogenic symbiont populations even within a single host, along a consistent gradient running the anterior-posterior axis of the symbiotic organ. Our results demonstrate that symbiont population structure across scales does not necessarily require host-mediated selection, as it can emerge as a result of ecological drift acting on both isogenic and unrelated competitors. Our findings illuminate the processes that might affect symbiont transmission, coinfection, and population structure in nature, which can drive the evolution of host–microbe symbioses and microbe–microbe interactions within host-associated microbiomes.

BACKGROUND Patients undergoing ileal pouch-anal anastomosis (IPAA) for inflammatory bowel disease (IBD) may experience post-operative inflammation of the ileal pouch (pouchitis) or rectal cuff (cuffitis). Post-operative pelvic floor dysfunction has previously been associated with inflammatory pouch outcomes. Furthermore, our recent pilot study identified an association between abnormal pre-operative anorectal manometry (ARM) and post-operative pouch ulceration and cuffitis; however, we did not adjust for covariates due to sample size and did not assess composite outcomes of pouch inflammation. In this expanded study, we aimed to further assess whether pre-operative pelvic floor dysfunction defined by abnormal anal sphincter function on ARM is associated with post-operative pouch and cuff inflammation. METHODS This historical cohort study assessed IBD patients who underwent pre-operative ARM with completion of their IPAA surgical series January 2009 - December 2024. Patients were divided into two groups—normal versus abnormal pelvic floor function—based on ARM prior to completion of IPAA surgical series. The two primary outcomes were a composite outcome of endoscopic inflammatory pouch diseases (EIPD) and an outcome of rectal cuffitis after the peri-operative period. Secondary outcomes included individual components of the composite primary outcome. Multivariable logistic regression was used to assess primary outcomes (EIPD and cuffitis) while controlling for covariates. RESULTS A total of 179 patients were included in this study, 46 (25.7%) in the abnormal ARM group and 133 (74.3%) in the normal ARM group. Cohorts had similar demographic and pre-operative characteristics except for gender; there was a higher proportion of females in the abnormal ARM group (63.0% versus 45.1%; p = 0.036). Median follow-up time after IPAA was 2.88 years for the abnormal ARM group and 3.61 years for the normal ARM group (p = 0.347). In total, 72 (40.2%) patients developed cuffitis and 61 (34.1%) developed EIPD. In multivariable regression, patients with abnormal ARM had a higher risk of cuffitis (OR 2.17; 95% CI 1.05-4.35; p = 0.037; Table 1) but not EIPD (p = 0.427). Secondary outcomes were similar between groups apart from diffuse pouch inflammation, which was more common in patients with abnormal ARM (p = 0.024; Table 2). DISCUSSION Abnormal pre-operative ARM was associated with post-operative cuffitis in IPAA patients after adjusting for potential confounders, which aligns with results from our pilot study. However, there was no significant association with EIPD. ARM prior to completion of IPAA surgical series could potentially be utilized to predict some inflammatory complications in select patients, but the specific associations between pre-operative ARM and endoscopic outcomes as well as the underlying mechanisms merit further investigation.

Host-associated microbiomes vary greatly in composition both within and between host individuals, providing the raw material for natural selection to act on host-microbe associations. Nonetheless, the drivers of compositional heterogeneity in host-associated microbiomes have only rarely been examined. To understand how this heterogeneity arises, we utilize the squash bug, Anasa tristis, and its bacterial symbionts in the genus Caballeronia. We artificially modulate symbiont bottleneck size and strain diversity during colonization to demonstrate the significance of ecological drift, which causes stochastic fluctuations in community composition. Consistent with predictions from the neutral theory of biodiversity, ecological drift alone can account for heterogeneity in symbiont community composition between hosts, even when two strains are nearly genetically identical. When acting on competing, unrelated strains, ecological drift can maintain symbiont genetic diversity among different hosts by stochastically determining the dominant strain within each host. Finally, ecological drift mediates heterogeneity in isogenic symbiont populations even within a single host, along a consistent gradient running the anterior-posterior axis of the symbiotic organ. Our results demonstrate that symbiont population structure across scales does not necessarily require host-mediated selection, but emerges as a result of ecological drift acting on both isogenic and unrelated competitors. Our findings illuminate the processes that might affect symbiont transmission, coinfection, and population structure in nature, which can drive the evolution of host-microbe symbiosis and microbe-microbe interactions within host-associated microbiomes.