Friends, Foes, or Both? Context-Dependent Symbiosis in Sweat Bees and Associated Nematodes

Abstract

Host-symbiont interactions are traditionally classified as mutualistic, commensal, or parasitic. However, these rigid classifications frequently oversimplify symbioses, which often heavily depend on ecological and environmental context. Here, I explore the context-dependent nature of a symbiosis between the socially polymorphic sweat bee, Megalopta genalis, and its associated diplogastrid nematode, Acrostichus megaloptae. The position of this relationship along the mutualism, commensalism, parasitism spectrum remains unclear, and reasonable hypotheses exist for all three categories. To investigate the potential metabolic cost of the symbiosis for hosts across social structures, I quantified fat body reserves in queens, workers, and solitary reproductives in relation to nematode presence and load. No statistically significant relationship was detected, which suggests that there is little or no cost associated with the symbiosis for hosts. However, a weak negative trend between nematode load and fat body quantity in workers indicates that high nematode loads may impose costs, potentially reflecting a shift towards parasitism. Further work with larger sample sizes is needed to confirm this relationship. The bacterial and fungal diet of A. megaloptae also remains unknown. Nematode diet likely plays a large role in determining the nature of the symbiosis. As such, I developed a surface sterilization protocol to prepare nematodes for downstream gut sequencing to determine what they are consuming within brood cells. Finally, I developed a theoretical model to explore how nematode feeding under different conditions may affect developing bees. I find that the length of the nematode feeding window, microbial composition, and nematode load all have the potential to shift the symbiosis along the mutualism, commensalism, parasitism spectrum. The model also suggests that potentially mutualistic nematode behavior in brood cells may result in costly, parasitic outcomes for adult bees. This implies that the nature of the symbiosis may change across the life stage of the host. In sum, these results highlight the importance of viewing symbioses as context-dependent interactions shaped by ecological conditions and host life history.