Elevated Temperatures Disrupt Wolbachia-Induced Feminisation and Reshape Microbial Community Dynamics Across Generations in a Spider Host

Longitudinal microbial interactions within a host are challenging to study, leading to a focus on constructed microbial communities in vitro settings. Here, we take advantage of a naturally defined microbial community within a spider host to study how elevated temperatures influence microbial dynamics and phenotypes across host generations. The spider Mermessus fradeorum hosts up to five endosymbionts, including a Wolbachia strain, W1, which induces feminisation, causing genetic males to develop as phenotypic females, skewing sex ratios and promoting symbiont spread. Despite this, Wolbachia 1 persists at intermediate frequencies in wild populations. We hypothesised that elevated temperatures might reduce penetration of the feminisation phenotype, potentially by altering symbiont dynamics and maternal transmission. We exposed spiderlings co-infected with Wolbachia 1 to elevated temperatures for one generation and measured feminisation rate, symbiont transmission, and titre across three generations. Feminisation was unaffected in the exposed (F1) generation but declined in subsequent generations (F2, F3) that were not directly exposed. This multigenerational effect was linked to shifts in symbiont community dynamics: low feminisation coincided with high abundance of one symbiont, Rickettsiella, a decline in Wolbachia 1 transmission, and complete loss of another symbiont, Tisiphia. Our findings demonstrate how environmental history shapes the evolutionary stability of microbial communities and their induced phenotype in their natural host.