Abstract
Studies of the ecoimmunology of feral organisms can provide valuable insight into how host–pathogen dynamics change as organisms transition from human-managed conditions back into the wild. Honey bees (Apis mellifera Linnaeus) offer an ideal system to investigate these questions as colonies of these social insects often escape management and establish in the wild. While managed honey bee colonies have low probability of survival in the absence of disease treatments, feral colonies commonly survive in the wild, where pathogen pressures are expected to be higher due to the absence of disease treatments. Here, we investigate the role of pathogen infections [Deformed wing virus (DWV), Black queen cell virus (BQCV), and Nosema ceranae] and immune gene expression (defensin-1, hymenoptaecin, pgrp-lc, pgrp-s2, argonaute-2, vago) in the survival of feral and managed honey bee colonies. We surveyed a total of 25 pairs of feral and managed colonies over a 2-year period (2017–2018), recorded overwintering survival, and measured pathogen levels and immune gene expression using quantitative polymerase chain reaction (qPCR). Our results showed that feral colonies had higher levels of DWV but it was variable over time compared to managed colonies. Higher pathogen levels were associated with increased immune gene expression, with feral colonies showing higher expression in five out of the six examined immune genes for at least one sampling period. Further analysis revealed that differential expression of the genes hymenoptaecin and vago increased the odds of overwintering survival in managed and feral colonies. Our results revealed that feral colonies express immune genes at higher levels in response to high pathogen burdens, providing evidence for the role of feralization in altering pathogen landscapes and host immune responses.
Highlights
Feralization is the process by which previously domesticated organisms establish populations in the wild in the absence of anthropogenic influence (Gering et al, 2019a)
We investigate the role of pathogen infections and immune gene expression in the survival of feral and managed honey bees to answer the following questions: (1) are feral colonies reservoirs of pathogens with increased levels of pathogens compared to managed colonies?; (2) do increased pathogen levels lead to higher expression of immune genes in feral colonies than in managed colonies?; (3) is immune gene expression correlated with survival of honey bee colonies? Over a 2-year period, we sampled feral and managed colonies in the same landscapes with the participation of beekeepers who reported the location of colonies
Spearman’s correlations (ρ) revealed that Deformed wing virus (DWV) levels were positively correlated with the expression of hymenoptaecin in the spring (ρ = 0.32), but not significantly correlated with any other pathogen levels or immune genes, while Black queen cell virus (BQCV) levels were positively correlated with N. ceranae levels in the spring (ρ = 0.48)
Summary
Feralization is the process by which previously domesticated organisms establish populations in the wild in the absence of anthropogenic influence (Gering et al, 2019a). The increased fecundity and expanded geographic ranges that result from the domestication processes, often result in large uncontrolled populations of feral organisms harboring infections and serving as a bridge between domesticated and wild hosts (Bevins et al, 2014) This is the case of the feral swine (Sus scrofa domestica), a species that has high rates of reproduction, high pathogen loads, and overlaps in range with domestic pigs (S. scrofa domestica) and wild boars (S. scrofa) (Taylor et al, 1998; Hill et al, 2014). Previous studies have indicated that feral honey bee colonies may exhibit higher immune responses than managed colonies (Youngsteadt et al, 2015, but see Lowe et al, 2011) It is unclear how the expression of different immune phenotypes in managed and feral conditions is associated with colony survival and resistance or tolerance to parasites. We identified two immune genes that are associated with colony survival and that can potentially be used as biomarkers of health in honey bee colonies
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