Longitudinal survey reveals delayed effects of low gene expression on stingless bee colony health

Abstract

Bee populations are declining globally due to different environmental stressors, such as pathogens, malnutrition, and agrochemicals. Brazil is the home of hundreds of stingless bee species, some of them now considered endangered, though very little is known about the impact of disease on native bees. In Southern Brazil the endangered stingless bee Melipona quadrifasciata is affected by an annual syndrome that causes sudden death of workers, eventually leading colonies to collapse. Although novel viruses were found in foragers from diseased colonies, none has been consistently implicated in the outbreak. Here we conducted an integrative longitudinal survey on M. quadrifasciata managed colonies, measuring individual- and colony-level traits, to identify the causes behind the syndrome. We found that key genes related to xenobiotic metabolization, nutrition and immune responses are downregulated in foragers from colonies that became diseased two months later. The period that preceded the outbreak was also marked by pronounced forager weight loss as well as behavioural changes. Our findings reveal the syndrome may result from the stingless bee failure to respond to sublethal stressors and disruption of colony dynamics. These results support the proposition that worldwide bee mortality is influenced by a combination of diverse sublethal factors, and increase awareness of the long-term effects of genetic diversity erosion in stingless bee species, which can be enhancing their vulnerability to environmental stressors.