The mushroom body development and learning ability of adult honeybees are influenced by cold exposure during their early pupal stage

Abstract

The honeybees are the most important pollinator in the production of crops and fresh produce. Temperature affects the survival of honeybees, and determines the quality of their development, which is of great significance for beekeeping production. Yet, little was known about how does low temperature stress during development stage cause bee death and any sub-lethal effect on subsequent. Early pupal stage is the most sensitive stage to low temperature in pupal stage. In this study, early pupal broods were exposed to 20°C for 12, 16, 24, and 48 h, followed by incubation at 35°C until emergence. We found that 48 h of low temperature duration cause 70% of individual bees to die. Although the mortality at 12 and 16 h seems not very high, the association learning ability of the surviving individuals was greatly affected. The brain slices of honeybees showed that low temperature treatment could cause the brain development of honeybees to almost stop. Gene expression profiles between low temperature treatment groups (T24, T48) and the control revealed that 1,267 and 1,174 genes were differentially expressed respectively. Functional enrichment analysis of differentially expressed genes showed that the differential expression of Map3k9, Dhrs4, and Sod-2 genes on MAPK and peroxisome signaling pathway caused oxidative damage to the honeybee head. On the FoxO signal pathway, InsR and FoxO were upregulated, and JNK, Akt, and Bsk were downregulated; and on the insect hormone synthesis signal pathway, Phm and Spo genes were downregulated. Therefore, we speculate that low temperature stress affects hormone regulation. It was detected that the pathways related to the nervous system were Cholinergic synapse, Dopaminergic synapse, GABAergic synapse, Glutamatergic synapse, Serotonergic synapse, Neurotrophin signaling pathway, and Synaptic vesicle cycle. This implies that the synaptic development of honeybees is quite possibly greatly affected by low temperature stress. Understanding how low temperature stress affects the physiology of bee brain development and how it affects bee behavior provide a theoretical foundation for a deeper comprehension of the temperature adaptation mechanism that underlies the “stenothermic” development of social insects, and help to improve honeybee management strategies to ensure the healthy of colony.

Comparative transcriptomics uncovers apoptosis in brain impairment in newly pupated honeybee worker under cold stress

“…35℃ is considered the optimal temperature for honeybee development, and our previous studies have shown through tissue sections that brain development of new pupae stagnates after exposure to cold stress, and learning and memory are impaired in adults [20]. However, the physiological processes and molecular mechanisms behind this phenomenon of cold-stress effect have not been thoroughly investigated.…”

“…Deviation from the optimal temperature during development can result in abnormal development of honeybee broods, including abnormal external morphology of adult honeybee (proboscis, forewing, and hind leg) [17], and a shortened lifespan [18,19]. Due to the various evidence available, it is clear that cold stress can hinder the development of honeybee brains [20]. This includes a decline in the number of mushroom body synaptic complexes [21], leading to impaired learning, memory, and foraging abilities in adult honeybees after they emerge [20].…”

“…Due to the various evidence available, it is clear that cold stress can hinder the development of honeybee brains [20]. This includes a decline in the number of mushroom body synaptic complexes [21], leading to impaired learning, memory, and foraging abilities in adult honeybees after they emerge [20].…”

“…Based on our team's preliminary research, it has been found that cold stress can impede brain development in the new puape stage of Apis mellifera and lead to a signi cant reduction in the learning and memory abilities when they emerge [20], however, the mechanism by which brain development is impeded remains unclear. In this study, we conducted in-depth comparative exploitation of previously collected high-quality transcriptome data, using the trend analysis method, we were able to select the set of genes that conformed to a certain expression pattern (e.g., the expression continued to increase or decrease) in honeybee pupae head under prolongation of cold treatment, to reduce the complexity of the data and the di culty of the analysis and facilitate the discovery of key genes that responded to the cold stress during this certain developmental stage.…”

Drosophilalarvae demonstrate associative learning and memory in response to thermal conditioning

“…At the neural circuit level, it has been established that the brain region responsible for learning and memory formation in insects is the mushroom body (MB) [6,[12][13][14][15][16][17][18][19][20][21][22][23][24][25][26][27][28][29][30][31]. A complete connectome of the larval brain [32] as well as the specific neural circuit responsible for olfactory memory [33] have been recently mapped.…”