Developmental environment shapes honeybee worker response to virus infection

Alexander Walton,Adam G Dolezal,Amy L Toth

doi:10.1038/s41598-021-93199-4

Alexander Walton, Adam G Dolezal + Show 1 more

Open Access

https://doi.org/10.1038/s41598-021-93199-4

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Abstract

The consequences of early-life experiences are far reaching. In particular, the social and nutritional environments that developing animals experience can shape their adult phenotypes. In honeybees, larval nutrition determines the eventual social roles of adults as reproductive queens or sterile workers. However, little is known about the effects of developmental nutrition on important adult worker phenotypes such as disease resilience. In this study, we manipulated worker developmental nutrition in two distinct ways under semi-natural field conditions. In the first experiment, we restricted access to nutrition via social isolation by temporarily preventing alloparental care. In the second experiment, we altered the diet quality experienced by the entire colony, leading to adult bees that had developed entirely in a nutritionally restricted environment. When bees from these two experiments reached the adult stage, we challenged them with a common bee virus, Israeli acute paralysis virus (IAPV) and compared mortality, body condition, and the expression of immune genes across diet and viral inoculation treatments. Our findings show that both forms of early life nutritional stress, whether induced by lack of alloparental care or diet quality restriction, significantly reduced bees’ resilience to virus infection and affected the expression of several key genes related to immune function. These results extend our understanding of how early life nutritional environment can affect phenotypes relevant to health and highlight the importance of considering how nutritional stress can be profound even when filtered through a social group. These results also provide important insights into how nutritional stress can affect honeybee health on a longer time scale and its potential to interact with other forms of stress (i.e. disease).

Highlights

Pathogen pressure, leading to increased morbidity and m ortality[29,30,31,32]
Offer the opportunity to study how nutritional differences are manifest through social feeding, considering how the filter of a large social group connects individual and group-level resource acquisition
We demonstrate how two different forms of socially-mediated developmental nutritional stress affect response to adult virus exposure and gene expression to affect a critical managed pollinator

Summary

Introduction

Pathogen pressure, leading to increased morbidity and m ortality[29,30,31,32]. An improved adult diet could mitigate these effects by maintaining immunocompetence[33]; for example, the detrimental effects of the microsporidian gut parasite Nosema ceranae can be offset by pollen quantity[34], quality, and diversity[35]. We manipulated colony-level diet by feeding experimental colonies only a high- or low-quality pollen source, producing colonies that experienced longer-term differential nutrition. In both cases, we predicted that the manipulations would be subtle enough to still allow production of seemingly-normal adult workers, but with increased sensitivity to infection, likely through modulation of immune responsiveness. We present evidence that both forms of stress significantly reduce bees’ resilience to virus infection These findings have important ramifications to our understanding of how developmental nutrition affects pathogen responses, within the complex network of environmental stressors faced by pollinators

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