Microbiome composition and turnover in the face of complex lifecycles and bottlenecks: insights through the study of dung beetles.

Abstract

Microbiome composition and function often change throughout a host's life cycle, reflecting shifts in the ecological niche of the host. The mechanisms that establish these relationships are therefore important dimensions of host ecology and evolution; yet, their nature remains poorly understood. Here, we sought to investigate the microbial communities associated with the complex life cycle of the dung beetle Onthophagus taurus and the relative contributions of host life stage, sex, and environment in determining microbiome assembly. We find that O. taurus plays host to a diverse microbiota that undergo drastic community shifts throughout host development, influenced by host life stage, environmental microbiota, and, to a lesser degree, sex. Contrary to predictions, we found that egg and pupal stages-despite the absence of a digestive tract or defined microbe-storing organs-do not constrain microbial maintenance, while host-constructed environments, such as a maternally derived fecal pellet or the pupal chamber constructed by late larvae, may still serve as complementary microbial refugia for select taxa. Lastly, we identify a small community of putative core microbiota likely to shape host development and fitness. Our results provide important insights into mechanisms employed by solitary organisms to assemble, maintain, and adjust beneficial microbiota to confront life-stage-specific needs and challenges.

Importance: As the influence of symbionts on host ecology, evolution, and development has become more apparent so has the importance of understanding how hosts facilitate the reliable maintenance of their interactions with these symbionts. A growing body of work has thus begun to identify diverse behaviors and physiological mechanisms underpinning the selective colonization of beneficial symbionts across a range of host taxa. Yet, how organisms with complex life cycles, such as holometabolous insects, establish and maintain key symbionts remains poorly understood. This is particularly interesting considering the drastic transformations of both internal and external host morphology, and the ecological niche shifts in diet and environment, that are the hallmark of metamorphosis. This work investigates the dynamic changes of the microbiota associated with the complex life cycle and host-constructed environments of the bull-headed dung beetle, Onthophagus taurus, a useful model for understanding how organisms may maintain and modulate their microbiota across development.