Cooperation and Conflict Within the Microbiota and Their Effects On Animal Hosts

Abstract

Symbioses between animals and microbes are ubiquitous, and often have drastic fitness effects on both parties. A rapidly growing body of research now shows that many of these effects are driven by social interactions among the symbionts. For instance, microbes frequently cooperate by producing shareable "public goods" that can mediate both virulence and host-beneficial functions. Conversely, hosts often exert control over symbionts by targeting their social interactions. Despite this pivotal role, we have only started to uncover the full diversity of microbial interactions, and many of the factors that shape variation in their effects on host function and evolution across different symbioses remain elusive. Here, we (i) review the known diversity of microbial interactions across different symbioses, and (ii) argue that variation in their nature and impact is often determined by differences in symbiont diversity. In particular, we first give a primer on the social lives of microbes, and then discuss how intraspecific and interspecific interactions among microbial symbionts affect -and are affected by -their host. Subsequently, we move to the evolution of symbiosis, and discuss the role of microbial interactions in symbioses that feature only few versus many different symbiont species. We show that symbiont-rich symbioses are shaped by strong interspecific competition, which selects against many host-beneficial forms of microbial cooperation, and thereby limits the scope for the evolution of strong host-symbiont dependencies. Conversely, symbioses involving only few symbiont species are often characterized by forms of microbial cooperation that mediate host-beneficial services, a situation that increases the scope for the evolution of host-symbiont dependencies. Overall, we infer that the explicit consideration of social dynamics within symbiont communities of varying complexity is crucial to advance our understanding of how microbes shape animal function and evolution.

Fungus-growing insects host a distinctive microbiota apparently adapted to the fungiculture environment

“…It also remains to be investigated the likelihood, extent, and metabolic outcomes of interactions occurring among bacterial populations within the FGI microbiota 81 . For instance, the abundance of pathways related to antimicrobials biosynthesis (Fig.…”

“…For instance, the abundance of pathways related to antimicrobials biosynthesis (Fig. 5 ) points to several viable interactions, including either competition among bacterial populations, between the microbiota and the fungal symbiont, or cooperation for defending the symbiosis against pathogens 81 , 82 . Also insightful would be to analyze the distribution, diversity, and stability of bacterial populations across the gradient of nutrients that derive from plant biomass metabolism by the fungal symbiont 82 – 84 .…”

Alteration of gut microbiota with a broad-spectrum antibiotic does not impair maternal care in the European earwig

“…Gut microbes were expected to directly drive the expression of parental care, because enforcing the expression of this social behaviour may allow symbionts to reach new hosts (i.e. offspring) that are typically young (thus offering long-lived habitats), display poor immune defences (thus facilitating bacterial establishment and development [63]) and harbour only a few resident microbes (thus limiting the risk of competition within the microbiome [29]). This absence of a link between rifampicin and maternal care may first suggest that earwig parental care is shaped by microbes that are non-sensitive to rifampicin.…”

Extracting the GEMs: Genotype, Environment, and Microbiome Interactions Shaping Host Phenotypes

“…On the other hand, fluctuating selection driven by sufficient temporal or spatial heterogeneity may hamper the fixation of MAPs in a population, or over multiple generations. It also important to understand the mechanisms that maintain cooperation between host and microbiome and prevent the emergence of cheating phenotypes ( Figueiredo and Kramer, 2020 ). For example, it has been shown that AMF and host use reciprocal rewards to stabilize beneficial interactions ( Kiers et al, 2011 ).…”