Warmer winters are associated with lower levels of the cryoprotectant glycerol, a slower decrease in vitellogenin expression and reduced virus infections in winter honeybees.

Within the context of climate change, winter temperatures at high latitudes are predicted to rise faster than summer temperatures. This phenomenon is expected to negatively affect the diapause performance and survival of insects, since they largely rely on low temperatures to lower their metabolism and preserve energy. However, some insects like honeybees, remain relatively active during the winter and elevate their metabolic rate to produce endothermic heat when temperatures drop. Warming winters are thus expected to improve overwintering performance of honeybees. In order to verify this hypothesis, for two consecutive years, we exposed honeybee colonies to either a mild or cold winter. We then monitored the influence of wintering conditions on several parameters of honeybee overwintering physiology, such as levels of the cryoprotectant glycerol, expression levels of immune and antioxidant genes, and genes encoding multifunctional proteins, including vitellogenin, which promotes bee longevity. Winter conditions had no effect on the expression of antioxidant genes, and genes related to immunity were not consistently affected. However, mild winters were consistently associated with a lower investment in glycerol synthesis and a higher expression of fat body genes, especially apidaecin and vitellogenin. Finally, while we found that viral loads generally decreased through the winter, this trend was more pronounced under mild winter conditions. In conclusion, and without considering how warming temperatures might affect other aspects of honeybee biology before overwintering, our data suggest that warming temperatures will likely benefit honeybee vitality by notably reducing their viral loads over the winter.

Honeybee lifespan: the critical role of pre-foraging stage.

Assessing the various anthropogenic pressures imposed on honeybees requires characterizing the patterns and drivers of natural mortality. Using automated lifelong individual monitoring devices, we monitored worker bees in different geographical, seasonal and colony contexts creating a broad range of hive conditions. We measured their life-history traits and notably assessed whether lifespan is influenced by pre-foraging flight experience. Our results show that the age at the first flight and onset of foraging are critical factors that determine, to a large extent, lifespan. Most importantly, our results indicate that a large proportion (40%) of the bees die during pre-foraging stage, and for those surviving, the elapsed time and flight experience between the first flight and the onset of foraging is of paramount importance to maximize the number of days spent foraging. Once in the foraging stage, individuals experience a constant mortality risk of 9% and 36% per hour of foraging and per foraging day, respectively. In conclusion, the pre-foraging stage during which bees perform orientation flights is a critical driver of bee lifespan. We believe these data on the natural mortality risks in honeybee workers will help assess the impact of anthropogenic pressures on bees.

Honey bee aggression supports a link between gene regulation and behavioral evolution.

A prominent theory states that animal phenotypes arise by evolutionary changes in gene regulation, but the extent to which this theory holds true for behavioral evolution is not known. Because "nature and nurture" are now understood to involve hereditary and environmental influences on gene expression, we studied whether environmental influences on a behavioral phenotype, i.e., aggression, could have evolved into inherited differences via changes in gene expression. Here, with microarray analysis of honey bees, we show that aggression-related genes with inherited patterns of brain expression are also environmentally regulated. There were expression differences in the brain for hundreds of genes between the highly aggressive Africanized honey bee compared with European honey bee (EHB) subspecies. Similar results were obtained for EHB in response to exposure to alarm pheromone (which provokes aggression) and when comparing old and young bees (aggressive tendencies increase with age). There was significant overlap of the gene lists generated from these three microarray experiments. Moreover, there was statistical enrichment of several of the same cis regulatory motifs in promoters of genes on all three gene lists. Aggression shows a remarkably robust brain molecular signature regardless of whether it occurs because of inherited, age-related, or environmental (social) factors. It appears that one element in the evolution of different degrees of aggressive behavior in honey bees involved changes in regulation of genes that mediate the response to alarm pheromone.