The road to the darkening of insects: Why do locusts change their temperament drastically after gathering into swarms?

Locusts are one of the major global agricultural pests, often bringing devastating blows to agricultural production and the ecological environment. According to the website of the Food and Agriculture Organization of the United Nations in 2020, as of that time, the worst desert locust plague in 25 years had swept across more than 20 countries in Africa and Asia, with a global affected area of ​​more than 16 million square kilometers, directly threatening the food security of about 19 million local people. In February 2023, the locust plague swept the region again, causing heavy losses. The harm of migratory locusts has existed since ancient times. From 707 BC to 1935, there were more than 800 clearly recorded locust plagues in my country. On average, there was a regional disaster every 2 to 3 years, and a large-scale locust plague that swept across most of China every 5 to 7 years.

Solitary locusts are green all over and hide in the grass. They only come into contact with each other when mating. Most of the time they are "lone rangers". They have weak flying ability and a small range of activities, and are basically not destructive. In fact, only when locusts change from low-density solitary to high-density gregarious can a locust plague break out.

Once the scattered locusts gather into a swarm, their appearance and temperament change greatly. The swarms of locusts will change color within a few hours, and their body color will change from green to dark brown, with the back turning black and the abdomen turning brown. In the locust-infested areas, people can often see a mass of black locusts. Social locusts show characteristics such as high density, large appetite, and strong flying ability. A locust swarm in an area of ​​one kilometer can accommodate 80 million adult locusts. These locusts have an amazing appetite and can eat 500 tons of food every day, which is equivalent to the food rations of 35,000 people. Social locusts have super strong flying ability and can fly hundreds or even thousands of kilometers, so once a locust swarm is formed, the degree and scope of damage are very large.

So, how do migratory locusts transform from solitary to gregarious? The mechanism of migratory locust metamorphosis has always been one of the major scientific issues of great concern to the international entomology community. The team of Academician Kang Le from the Institute of Zoology, Chinese Academy of Sciences, has conducted in-depth research for more than 20 years to solve this problem. The research results of "Research on the Molecular Regulatory Mechanism of Migratory Locust Metamorphosis" led by Academician Kang Le won the second prize of the National Natural Science Award in 2017.

The most fundamental way to find methods and drugs to prevent and control locust plagues is to thoroughly study the mechanism that induces insect gregariousness. Through years of research, the team of Academician Kang Le has developed new technologies and methods such as gene chips and small RNA technology, and conducted a comprehensive comparative analysis of the gene expression levels, epigenetic regulation, transcriptome and metabolome of solitary and gregarious locusts. It was found that the process of locust mutation involves a complex regulatory network with multiple genes and multiple levels, which ultimately leads to significant phenotypic differences between solitary and gregarious locusts in terms of behavior, migration, body color, reproduction, development, defense and feeding.

The first thing to study here is to understand how the metamorphosis of the two types of locusts (solitary and gregarious) is initiated and maintained. Kang Le's team found that the initiation of metamorphosis of locusts first starts with the sense of smell. Two types of chemical odor-sensing genes related to smell initiate locust aggregation by regulating the sensitivity of the locust's sense of smell. If substances that regulate these olfactory-related genes are found, green and environmentally friendly locust biopesticides can be screened. A series of studies have shown that the initiation of locust swarm aggregation also involves a variety of chemical substances, such as dopamine, acetylcarnitine, etc. Among them, dopamine is the key regulatory factor in initiating locust swarming. The expression of dopamine in gregarious locusts is significantly increased, regulating a series of central nervous signal pathways, which is equivalent to notifying various parts of the locust's body - take your positions and start metamorphosis!

The long-distance migration of swarms of locusts is the main cause of locust plagues. Through long-distance migration, locust swarms can obtain sufficient food and find suitable places to lay eggs, which is conducive to the survival of the group and the reproduction of offspring. However, long-distance migration is very energy-consuming. In addition to eating a lot, gregarious locusts are also better than solitary locusts in terms of energy utilization efficiency. Kang Le's team found that gregarious locusts are "long-distance runners" who are suitable for long-term and long-distance flights, while solitary locusts are "sprinters" who are suitable for short-distance jumping to avoid natural enemies. Some neuropeptides play an important role in improving the flight ability of gregarious locusts. For example, ester mobilization hormone-related neuropeptides are involved in the oxidation and utilization of esters, solving the problem of efficient energy utilization in long-distance flight.

The melanization of body color in the metamorphosis of locusts is also a very interesting study. Researchers have found that the change in body color is actually a group defense mechanism of gregarious locusts. Solitary locusts are green to protect themselves in the grass, while gregarious locusts are used to ostentatiousness and no longer need to camouflage and hide. Therefore, green has no protective significance. The gregarious locusts turn "melanized" and secrete toxic ingredients in their bodies. The black and brown body color is also a warning color, in order to send a warning signal to natural enemies - don't eat me, I'm poisonous!

As for why locusts can "blacken", people previously speculated that it was due to the deposition of melanin. Until 2019, the Kang Le team found that the black and brown body color is not due to the increase of melanin, but when the density of locusts increases, the expression levels of many genes in the locusts will change accordingly. The expression level of a gene that synthesizes β-carotene binding protein will increase significantly, and a large amount of β-carotene binding protein will combine with β-carotene to form red pigment, which will then mix with the green substance in the locust to form black. It turns out that there is a natural "palette" in the locust.

These studies have been highly recognized by international peers and are considered to be the most encouraging breakthrough research in the field in the past decade. They are not only of great significance for understanding the response and adaptability of organisms to a changing environment, but also provide a series of new ideas and solutions for the prevention and control of locust plagues.

(Text: Tang Bo, Research Librarian of Zhongguancun Guoke Modern Agricultural Industry Science and Technology Innovation Research Institute. Expert: Zhao Xumao, Researcher of Lanzhou University School of Ecology)

China Association for Science and Technology Department of Science Popularization

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