Animal development in the microbial world: Re-thinking the conceptual framework

Abstract

Animals have evolved within the framework of the microbes and are constantly exposed to diverse microbiota. This dominance of the microbial world is forcing all fields of biology to question some of their most basic premises, with developmental biology being no exception. While animals under laboratory conditions can develop and live without microbes, they are far from normal, and would not survive under natural conditions, where their fitness would be strongly compromised. Since much of the undescribed biodiversity on Earth is microbial, any consideration of animal development in the absence of the recognition of microbes will be incomplete. Here, we show that animal development may never have been autonomous, rather it requires transient or persistent interactions with the microbial world. We propose that to formulate a comprehensive understanding of embryogenesis and post-embryonic development, we must recognize that symbiotic microbes provide important developmental signals and contribute in significant ways to phenotype production. This offers limitless opportunities for the field of developmental biology to expand.

Keywords: Development; Embryogenesis; Evolution; Microbiota; Symbiosis.

Figure 1.

Bosch and McFall-Ngai Incorporating coevolved symbioses into the hierarchy of life. The recognition that many, if not most,animals are metaorganisms, comprising host and associated microbial partners, drives a conceptual shift in our view of the hierarchy of life, one that reflects the nested nature of biological systems. Illustrated here is the hierarchy of the fully mature individual and its associated ecological context. Prior to the dawn of next-generation sequencing (‘pre-’), the increasing complexity of the hierarchical organization of biological systems was presumed to be linear, with ‘emergent properties’ arising with each successive level of organization. New data, resulting from advances in sequencing technology (‘post-’), have revealed that the biosphere comprises a more complex hierarchy, one that incorporates the inherent nesting of the macro- and microbial worlds. A holobiont is created through dynamic interactions between the host and microbial elements, through the trajectory of development, from fertilization through ontogeny.