Ecological and evolutionary dynamics of chlamydiae endosymbionts in social amoeba host communities

James G DuBose, Patricia Fiedorek, Mackenzie Hoogshagen, Donovan Clark, Alyssa Nolan, Hailee Gerner, Phong Nguyen, Kira Gibbs, Tamara S. Haselkorn

Endosymbiotic interactions have played fundamental roles in shaping the evolution of complex eukaryotes. However, how ecological processes shape endosymbioses that are still segregating in host populations have been less described. Here, we characterize the ecological and evolutionary dynamics of chlamydiae bacterial endosymbionts in dictyostelid social amoeba host communities. Our survey of over 1400 host isolates from across a 1200 km range revealed 41 unique chlamydiae haplotypes across 11 different host species, the prevalence of which significantly varied across host species and sampling locations. Patterns of chlamydiae phylogenetic divergence were not associated with geographic dissimilarity but were associated with patterns of host diversification, suggesting a shared evolutionary history and co-dispersal between some symbiont and host lineages. However, relatively few symbiont haplotypes showed both significant host specificity and high prevalence, indicating that most associations are not ecologically meaningful. Nonetheless, our laboratory passaging experiments showed that naturally occurring chlamydiae infections can be vertically transmitted across host generations. Finally, we found overall chlamydiae haplotype diversity was negatively associated with prevalence across host populations, mirroring the classic tension between selection and the influx of neutral variation due to ecological drift and stochastic environmental acquisition. To formalize this observation, we developed a stochastic differential equation model incorporating vertical and environmental symbiont transmission, as well as ecological selection and drift. This model recapitulated the observed diversity-prevalence relationship, and is consistent with a scenario in which most chlamydiae haplotypes are ecologically neutral and stochastically acquired, while relatively few are vertically transmitted and selectively relevant within their host populations.