Abstract
Social insects maximize resource acquisition and allocation through division of labor and associations with microbial symbionts. Colonies divide labor among castes and subcastes, where the plasticity of caste roles decreases in clades with higher social grades. Recent studies indicate that specific castes may also foster distinct gut microbiomes, suggesting synergies between division of labor and symbiosis. The social organization of a colony potentially partitions evolutionary persistent microbial partners to optimize symbioses and complement division of labor. However, research in this area has received limited attention. To elucidate if a structured microbiota is adaptive, we present three testable predictions to address consistent community structure, beneficial functions, and selection for microbiota that support caste roles. First, we posit that social insect groups spanning lower to higher social grades exhibit increasingly distinct caste microbiomes, suggesting that structured microbiomes may have evolved in parallel to social complexity. Second, we contend that the development of these microbiomes during colony maturation may clarify the extent to which they support division of labor. Third, we predict that mature social insect colonies with the most extreme division of labor demonstrate the strongest distinctions between caste microbiomes, carrying the greatest promise of insight into microbiome composition and function. Ultimately, we hypothesize that caste-specific microbiomes may enhance symbiotic benefits and the efficiency of division of labor, consequently maximizing fitness.
Highlights
Organisms are selected to optimize resource use through their own actions and interactions, in turn maximizing reproductive success
To begin to assess this hypothesis, we review division of labor in the social insects, known gut microbiota compositional differences between castes and subcastes, and the role of social interactions in influencing persistent gut microbiota
We hypothesize that hosts may organize and optimize the gut microbiota among colony members to increase the benefits of symbioses and social organization
Summary
Organisms are selected to optimize resource use through their own actions and interactions, in turn maximizing reproductive success. Social corbiculate bees, and clades of ants consistently host microbial phylotypes over evolutionary timescales, as indicated by patterns of phylogenetic congruence of microbial communities with hosts (Russell et al, 2009; Dietrich et al, 2014; Sanders et al, 2014; Kwong et al, 2017; Lukasik et al, 2017; Bourguignon et al, 2018; Sapountzis et al, 2019) This indicates vertical transmission across generations, most symbioses are characterized by the presence of at least some degree of host switching, suggesting that horizontal transmission persists across host clades (Koch et al, 2013; Sanders et al, 2014; Kwong et al, 2017; Bourguignon et al, 2018). The extensive evolutionary histories of hosts and symbionts are presumably facilitated by social interactions and insect physiological or morphological characteristics that promote specific microbial partners (c.f. Kwong and Moran, 2015; Lanan et al, 2016; Sapountzis et al, 2019)
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