The evolution of honey bee brains

Newswise — A new theory has been presented by scientists regarding the development of advanced brain functions and behaviors in insects of the Hymenoptera order. By comparing the Kenyon cells, a specific type of nerve cell, in the mushroom bodies of basic sawflies and complex honey bees, the team discovered that three distinct and specialized Kenyon cell subtypes in honey bees likely originated from one multifaceted subtype of Kenyon cell in a common ancestor. This study may offer insight into the evolution of our own advanced brain functions and behaviors in the future.

Do you consider yourself as "busy as a bee," a "social butterfly," or a "fly on the wall"? Interestingly, the use of insect behavior analogies may have more significance than just being fun idioms. Researching insects can not only shed light on the evolution of their behavior but also on the behavior of highly evolved animals, such as humans. Due to the complexity of mammalian brains, it is challenging to determine which behaviors and neural and genetic alterations have co-evolved over time. In contrast, insect brains are much less intricate, making them ideal models for scientific inquiry.

"Back in 2017, we published a report stating that as the behavioral diversity in Hymenoptera (a diverse and vast order of insects) increases, the complexity of Kenyon cell (KC) subtypes in mushroom bodies within their brains also increases," explained co-author of the current study, Professor Takeo Kubo from the Graduate School of Science at the University of Tokyo. "This implies that the more KC subtypes an insect has, the more intricate its brain and its potential behaviors become. However, we were uncertain about the evolutionary process behind the development of these distinct subtypes. This curiosity inspired our latest study."

The University of Tokyo and Japan’s National Agriculture and Food Research Organization (NARO) researchers selected two Hymenoptera species as representatives of different behaviors: the solitary turnip sawfly (with a single KC subtype) and the highly sophisticated, social honey bee (with three KC subtypes). Since the sawfly has a less developed brain, it is believed to possess some ancestral properties of the honey bee brain. To uncover the potential evolutionary paths between them, the scientists utilized transcriptome analysis to detect the gene expression profiles (the genetic activity) of the various KC subtypes and hypothesize their functions.

Assistant Professor Hiroki Kohno, co-author from the Graduate School of Science, expressed surprise at the discovery, saying, "I was amazed that each of the three KC subtypes in honey bees displayed a similar resemblance to the single KC subtype in the sawfly. Our initial comparative analysis of several genes led us to assume that additional KC subtypes had been added sequentially. However, it appears that they were separated from a multifunctional ancestral type through functional segregation and specialization." With an increase in the number of KC subtypes, each subtype acquired unique traits from an ancestral KC in almost equal measure. These properties were then altered in distinct ways, leading to the diverse functions they exhibit today.

The scientists aimed to find a particular behavioral instance where ancestral KC functions were evident in both the sawfly and the honey bee. To accomplish this, they taught sawflies to perform a standard honey bee behavioral test, where they were trained to connect an odor stimulus with a reward. Although initially challenging, the team was eventually successful in getting the sawflies to engage in the memory task. The researchers then manipulated a gene called CaMKII in sawfly larvae, which, in honey bees, is associated with the development of long-term memory, a KC function. As the larvae transformed into adults, their long-term memory was impaired, indicating that the gene has a similar role in both sawflies and honey bees. Although CaMKII was active across the entire single KC subtype in sawflies, it was selectively active in only one KC subtype in honey bees. This suggests that the role of CaMKII in long-term memory was transferred to the specific KC subtype in honey bees.

Despite the significant differences in size and complexity between insect and mammalian brains, there are similarities in function and the fundamental structure of the nervous system. This is why the model put forward in this study for the evolution and diversification of KC subtypes may contribute to a better understanding of the evolution of our own behavior. The team's next goal is to examine KC subtypes obtained in parallel with social behaviors, such as the honey bee's "waggle dance."

Takayoshi Kuwabara, doctoral student and lead author from the Graduate School of Science, expressed his desire to investigate whether the model proposed in this study is relevant to the evolution of other behaviors. According to him, there are many unknowns about the neural mechanisms that govern social behavior in insects, animals, and humans, and how it has evolved. He believes that this study is an innovative work in this area, and further research could potentially reveal more insights into the evolution of behavior.

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Paper Title:

Takayoshi Kuwabara, Hiroki Kohno, Masatsugu Hatakeyama, Takeo Kubo. Evolutionary dynamics of mushroom body Kenyon cell types in hymenopteran brains from multi-functional type to functionally specialized types. Science Advances. DOI: 10.1126/sciadv.add4201

Funding:

This research was supported by Grant-in-Aid for Scientific Research (B) 20H03300 (TKubo) and Grant-in-Aid for JSPS Fellows 21J20847 (TKuwabara).