Abdominal microbial communities in ants depend on colony membership rather than caste and are linked to colony productivity

Abstract

Gut bacteria aid their host in digestion and pathogen defense, and bacterial communities that differ in diversity or composition may vary in their ability to do so. Typically, the gut microbiomes of animals living in social groups converge as members share a nest environment and frequently interact. Social insect colonies, however, consist of individuals that differ in age, physiology, and behavior, traits that could affect gut communities or that expose the host to different bacteria, potentially leading to variation in the gut microbiome within colonies. Here we asked whether bacterial communities in the abdomen of Temnothorax nylanderi ants, composed largely of the gut microbiome, differ between different reproductive and behavioral castes. We compared microbiomes of queens, newly eclosed workers, brood carers, and foragers by high‐throughput 16S rRNA sequencing. Additionally, we sampled individuals from the same colonies twice, in the field and after 2 months of laboratory housing. To disentangle the effects of laboratory environment and season on microbial communities, additional colonies were collected at the same location after 2 months. There were no large differences between ant castes, although queens harbored more diverse microbial communities than workers. Instead, we found effects of colony, environment, and season on the abdominal microbiome. Interestingly, colonies with more diverse communities had produced more brood. Moreover, the queens' microbiome composition was linked to egg production. Although long‐term coevolution between social insects and gut bacteria has been repeatedly evidenced, our study is the first to find associations between abdominal microbiome characteristics and colony productivity in social insects.

Immune challenge reduces gut microbial diversity and triggers fertility-dependent gene expression changes in a social insect

“…Gut bacteria benefit their insect hosts in various ways, for example, by aiding in digestion [ 66 , 67 ], protecting against pathogens [ 68 ] and increasing fecundity [ 69 ]. Diversity of the colony gut microbiome is linked to high colony productivity in another Temnothorax species, T. nylanderi [ 70 ]. Thus, a turnover of the normal gut microbiome following a provocation of the immune system somewhere else in the body could present an additional cost to immune responses in insects, next to the direct energetic costs of immune activity.…”

Bacterial Composition and Diversity of the Digestive Tract of Odontomachus monticola Emery and Ectomomyrmex javanus Mayr

“…Each pooled sample was homogenized using sterile pestles and incubated at 37 °C overnight in the lysozyme to lyse the cell walls of Gram-positive bacteria [ 26 ]. Genomic DNA was extracted using DNeasy Blood & Tissue extraction kit (Tian Gen, Beijing, China) according to the manufacturer’s instructions.…”

Applying the core microbiome to understand host–microbe systems

“…For example, the relative abundance of the genera Oscillospira and Coprococcus ocillate predictably with season in the gut microbiome of Red squirrels (Ren et al, 2017); Lactobacillus, Alistipes and Helicobacter seasonally fluctuate in wild mice (Maurice et al, 2015); and Lactobacillus and Bartonella predictably increase over winter in the gut microbiomes of Honey bees (Kešnerová et al, 2020). The extent to which such dynamics are externally and internally driven are unclear, although laboratory studies show that seasonal shifts in at least some taxa are host controlled in response to changes in temperature/light stimuli (Carey, Walters, & Knight, 2013;Ferguson et al, 2018;Segers, Kaltenpoth, & Foitzik, 2019). These examples of seasonal variation at the host population level usually identify a small number of taxa that exhibit predictable dynamics, yet the temporal core can encompass many more species if it includes taxa that persist in a stable state within individuals, because priority effects during development can generate individualized microbiomes that are highly stable and resistant to invasion (Obadia et al, 2017) The temporal core can overlap with the common core when measured at the host population level.…”