Towards an Evolutionary Model of Animal-Associated Microbiomes

Abstract

Second-generation sequencing technologies have granted us greater access to the diversity and genetics of microbial communities that naturally reside endo- and ecto-symbiotically with animal hosts. Substantial research has emerged describing the diversity and broader trends that exist within and between host species and their associated microbial ecosystems, yet the application of these data to our evolutionary understanding of microbiomes appears fragmented. For the most part biological perspectives are based on limited observations of oversimplified communities, while mathematical and/or computational modeling of these concepts often lack biological precedence. In recognition of this disconnect, both fields have attempted to incorporate ecological theories, although their applicability is currently a subject of debate because most ecological theories were developed based on observations of macro-organisms and their ecosystems. For the purposes of this review, we attempt to transcend the biological, ecological and computational realms, drawing on extensive literature, to forge a useful framework that can, at a minimum be built upon, but ideally will shape the hypotheses of each field as they move forward. In evaluating the top-down selection pressures that are exerted on a microbiome we find cause to warrant reconsideration of the much-maligned theory of multi-level selection and reason that complexity must be underscored by modularity.

Keywords: animal; complexity; ecology; evolution; interdependency; microbiome; modularity; multi-level selection.

Figure 1.

Fitness Landscape. A 3-dimensional representation of a fitness landscape; used to describe the multiplicity of adaptive trajectories available to a species. These trajectories may lead to points of lower fitness, represented as a valley, or higher points of fitness, represented as a mountain, while neutral regions manifest as plateaus. While a clone would occupy a single point within the fitness landscape, a species is aclonal. Although best thought of in an additional dimension, for simplicity we have depicted a species (blue dots) as multiple clonal types surrounding the modal subpopulation (circled in red). Adaptation arises when the modal subpopulation moves to a new position within the landscape although intraspecific genetic variation would enable tethered migrations from the modal genotype.

Figure 2.

The complexity of selective forces acting on the microbiome. Illustrates the multiplicity of factors influencing the evolutionary trajectories of the microbiome and their interplay as described in this review. Black arrows indicate influence, while red diamonds indicate checkpoints.