Microbially Mediated Chemical Ecology of Animals: A Review of Its Role in Conspecific Communication, Parasitism and Predation

Abstract

Microbial symbionts are nowadays considered of pivotal importance for animal life. Among the many processes where microorganisms are involved, an emerging research avenue focuses on their major role in driving the evolution of chemical communication in their hosts. Volatiles of bacterial origin may underlie chemical communication and the transfer of social information through signals, as well as inadvertent social information. We reviewed the role of microorganisms in animal communication between conspecifics, and, because the microbiome may cause beneficial as well as deleterious effects on their animal hosts, we also reviewed its role in determining the outcome of the interactions with parasites and predators. Finally, we paid special attention to the hypothetical role of predation and parasitism in driving the evolution of the animal microbiome. We highlighted the novelty of the theoretical framework derived from considering the microbiota of animals in scenarios of communication, parasitism, and predation. We aimed to encourage research in these areas, suggesting key predictions that need to be tested to better understand what is one of the main roles of bacteria in animal biology.

Keywords: bacteria; chemical communication; ectoparasite–host interaction; microbiome; predator–prey interaction; volatiles.

Figure 1

Diagram showing hypothetical influence of bacterial symbionts (green arrows) in scenarios of social communication, parasitism, and predation. These influences could be directly due to either bacterial metabolism or products with antimicrobial or antipredatory properties (solid arrows), or indirectly through their effects on host characteristics (i.e., health, scents, metabolism, immunity, and hormones) (dashed green arrows). Bacterial symbionts contribute to social information that is received by conspecifics or heterospecifics, including parasites and predators. The negative effects of parasites and predators (red arrow) would be directly counteracted by defensive products of bacterial origin, or indirectly by host defensive traits that are also influenced by bacteria (continuous and dashed green arrows connecting the host with parasites and predators). These negative effects however will be enhanced by eavesdropping on inadvertent social information directly or indirectly mediated by host microbial symbionts and, thus, parasites and predators will also influence the symbiotic association between animals and microorganisms. Pathogenic parasites could also influence health and, consequently, bacterial symbionts of their victims, and, thus, parasites could indirectly affect conspecific communication. Numbers refer to main sections in the text where that relationships are covered. Symbols courtesy of the Integration and Application Network, University of Maryland (ian.umces.edu/symbols/) and freepik.com (accessed on 5 February 2021).