Beetle chemical defense gland offers clues to complex organ evolution – sciencedaily


Staphylins are among the chemists of the insect world, concocting harmful compounds in their bodies that are armed to ward off predators, allowing beetles to survive in the leaf litter and soil of the planet’s ecosystems. December 9 in the newspaper Cell, researchers studying a species of staphylins report how two distinct cell types came together to form a gland specialized in the manufacture and secretion of these defensive cocktails. The work has implications for mapping the evolution of more sophisticated organs found in the animal kingdom, including humans.

“These beetles are fantastic models for understanding how new types of ecological relationships emerge during evolution through changes at the molecular, cellular and behavioral levels,” says lead author Joseph Parker (@Pselaphinae) of the California Institute of Technology. “As part of this question, we’re very interested in how staphylins have reconstructed these glandular structures in their abdomen, which are made up of different types of cells that work together. These structures embody a major conundrum. : how complex organs evolve which are often made up of many different cell types that seem to cooperate seamlessly with each other. How this cooperativity emerges during evolution is difficult to explain. “

Parker’s lab focuses on ragweeds in part because of their ability to carve niches in many different ecosystems, from the earth to the interior of ant colonies. They were able to survive in the presence of other insects, such as ants, thanks to glands in their abdomen that release a defensive chemical compound that triggers pain receptors. Beetles have extremely flexible bodies and can apply these chemical cocktails directly to predators for self-defense.

The species of staphylins that was the subject of this research, Dalotia coriaria, has what’s called a tergal gland in its abdomen that releases a cocktail made up of two types of compounds: benzoquinones, which are very toxic but inherently strong, and solvents, a mixture of fatty acids derived from a alkane and three esters. These latter compounds in themselves are benign, but they convert the benzoquinones into a weapon by dissolving them.

Parker’s group investigated the tergal gland and discovered two types of cells involved in a biosynthetic division of labor. “One type of cell makes benzoquinones and the other makes solvents,” Parker explains. “Both are necessary to create a functional secretion that confers fitness.”

In the study, the researchers used single-cell transcriptomics of the abdominal segments of beetles to discover new enzymatic pathways that allow the creation of these substances in each cell type. They then used those findings to dig deeper, exploring how each cell type’s pathway was constructed from components that worked in other older cell types elsewhere in the beetle. “We were able to discover the biosynthetic pathways in each type of cell and then were able to ask how these pathways were stitched together during evolution,” Parker notes.

Remarkably, one of the cell types – the solvent cells that make the alkane and esters – turned out to be a hybrid of cells comprising the beetle’s exoskeleton and two ancient types of metabolic cells that make and store lipids. and produce pheromones. “The beetle recruited a major gene expression program from these ancient types of metabolic cells and installed it in an area of ​​the cuticle, creating a gland,” Parker explains.

Other experiments, including placing the beetles in battle arenas with ants, revealed that when the solvent or benzoquinone pathway was destroyed, the beetles lost their defensive abilities. This suggests that under natural selection both types of cells are required to confer the chemical defense system of beetles. Investigators also found that the compound made by the tergal gland had antimicrobial properties, further increasing the fitness of the gland.

The authors believe that the gland evolved via coevolution between the two types of cells. “The solvent cells created a niche for a second cell type to produce the solid benzoquinones, which could dissolve in the alkane and esters. A highly toxic secretion emerged that dramatically increased the fitness of the gland, locking the two types of cells in a unit where they cooperate. Essentially, a new organ has emerged, “says Parker.

“In the animal tree of life, you see complex multicellular organs made up of many different cell types working collectively,” Parker concludes. “Think of something like the mammalian eye, which has about 70 different cell types all working together to enable our visual system. The scenario that we find in the tergal gland – an organ made up of two types of cells – you can imagine could go through other cycles as cell types create niches to add new ones, ultimately generating truly elaborate multicellular complexity. ”

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