Manipulating nest architecture reveals three-dimensional building strategies and colony resilience in honeybees.

Form follows function throughout the development of an organism. This principle should apply beyond the organism to the nests they build, but empirical studies are lacking. Honeybees provide a uniquely suited system to study nest form and function throughout development because we can image the three-dimensional structure repeatedly and non-destructively. Here, we tracked nest-wide comb growth in six colonies over 45 days (control colonies) and found that colonies have a stereotypical process of development that maintains a spheroid nest shape. To experimentally test if nest structure is important for colony function, we shuffled the nests of an additional six colonies, weekly rearranging the comb positions and orientations (shuffled colonies). Surprisingly, we found no differences between control and shuffled colonies in multiple colony performance metrics-worker population, comb area, hive weight and nest temperature. However, using predictive modelling to examine how workers allocate comb to expand their nests, we show that shuffled colonies compensate for these disruptions by accounting for the three-dimensional structure to reconnect their nest. This suggests that nest architecture is more flexible than previously thought, and that superorganisms have mechanisms to compensate for drastic architectural perturbations and maintain colony function.

Azteca ants maintain unique microbiomes across functionally distinct nest chambers.

The microbiome of built structures has considerable influence over an inhabitant's well-being, yet the vast majority of research has focused on human-built structures. Ants are well-known architects, capable of constructing elaborate dwellings, the microbiome of which is underexplored. Here, we explore the bacterial and fungal microbiomes in functionally distinct chambers within and outside the nests of Azteca alfari ants in Cecropia peltata trees. We predicted that A. alfari colonies (1) maintain distinct microbiomes within their nests compared to the surrounding environment, (2) maintain distinct microbiomes among nest chambers used for different functions, and (3) limit both ant and plant pathogens inside their nests. In support of these predictions, we found that internal and external nest sampling locations had distinct microbial communities, and A. alfari maintained lower bacterial richness in their 'nurseries'. While putative animal pathogens were suppressed in chambers that ants actively inhabited, putative plant pathogens were not, which does not support our hypothesis that A. alfari defends its host trees against microbial antagonists. Our results show that ants influence microbial communities inside their nests similar to studies of human homes. Unlike humans, ants limit the bacteria in their nurseries and potentially prevent the build-up of insect-infecting pathogens. These results highlight the importance of documenting how indoor microbiomes differ among species, which might improve our understanding of how to promote indoor health in human dwellings.

Ant-plant sociometry in the Azteca-Cecropia mutualism.

A holistic understanding of superorganism biology requires study of colony sociometry, or the quantitative relationships among growth, nest architecture, morphology, and behavior. For ant colonies that obligately nest within plant hosts, their sociometry is likely intertwined with the plant, which has implications for the evolution, strength, and stability of the mutualism. In the Azteca-Cecropia mutualism, plants provide ants with food rewards and hollow stems for nesting in return for protection from herbivores. Several interesting questions arise when considering ant-plant sociometry: are colony growth and plant growth synchronized? How do colonies distribute themselves within the stem of their host plant? How do plant traits influence worker morphology? How is collective personality related to tree structure, nest organization, and worker morphology? To address these questions, we investigated patterns within and relationships among five major sociometric categories of colonies in the field - plant traits, colony size, nest organization, worker morphology, and collective personality. We found that colony sociometry was intimately intertwined with host plant traits. Colony and plant growth rates were synchronized, suggesting that positive feedback between plant and colony growth stabilizes the mutualism. The colony's distribution inside the host tree tended to follow leaf growth, with most workers, brood, and the queen in the top half of the tree. Worker morphology correlated with plant size instead of colony size or age, which suggests that plant traits influence worker development. Colony personality was independent of colony distribution and tree structure but may correlate with worker size such that colonies with smaller, less variable workers had more aggressive personalities. This study provides insights into how ant-plant structural relationships may contribute to plant protection and the strength of mutualisms.