Fertility costs of cryptic viral infections in a model social insect

Abstract

Declining global insect populations emphasize the importance of understanding the drivers underlying reductions in insect fitness. Many insects are subject to a trade-off between reproduction and immune activity, meaning that infections can have indirect impacts on fecundity, even in the absence of overt symptoms. While eusocial insects have escaped a broader trade-off between reproduction and lifespan, our results suggest that honey bees, a model Hymenopteran, are susceptible to reproduction-immunity compromises. We report that natural viral infection is associated with decreased ovary mass and upregulation of heat-shock proteins (HSPs) which are part of the honey bee's antiviral response. Failed (poor quality) queens sampled from a wide geographic range have higher levels of viral infection, smaller ovaries, and altered ovarian protein composition, with over 20% of proteins differentially expressed. Significantly reduced levels of the yolk-protein precursor vitellogenin in the ovaries indicate a direct decline in fertility. We experimentally infected queens with Israeli acute paralysis virus and, as expected, infected queens exhibited significantly lower vitellogenin expression and higher HSP expression, confirming a causal relationship between viral infection and genes involved in fertility and immunity. The link between ovary size and queen failure could not be explained by other abiotic stressors. These findings suggest that viral infections occurring naturally in the field are compromising reproductive success, even among social insects.