A beetle’s poisonous punch is helping to uncover how new types of cells can arise and co-evolve to create organs – and these mechanisms may apply to more complex organs in animals, including humans.

A fundamental challenge that multicellular animals face is how to get different cell types to work together so that a higher-level function, such as that of an organ, emerges from their interactions, says Joe Parker at the California Institute of Technology. Yet biologists know relatively little about how this happens.

Many organs that are common across animal groups are complex and evolutionarily ancient, making it hard to unpick their origins. But the defence glands of a family of insects known as rove beetles are simpler and only about 100 million years old – much younger than ancient cell types, such as those for body fat or compound eyes, that all insects possess.

One species, the greenhouse rove beetle (Dalotia coriaria), has a pair of glands in its abdomen – composed of only two cell types – that secrete a solid toxin dissolved in an oily fluid. If attacked by a predator such as an ant, the beetle whips its flexible abdomen around and smacks a dab of this cocktail in the ant’s face. The toxin triggers the ant’s pain receptors, forcing it to retreat.

To uncover the evolutionary roots of this defence mechanism, Parker and his team used a technique called single-cell RNA sequencing to analyse the gene activity in the two cell types. This showed that one type makes the solvent, while the other makes the toxin.

Comparisons with gene activity in other body cells revealed that the solvent cells had adapted existing suites of genes that govern cells elsewhere in the beetle’s body: those that make up tissues in its equivalent of the liver and fat, as well as those that make chemical signals called pheromones. This remodelling allowed the new cell type to make oily solvent components.

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The toxin cells, meanwhile, had repurposed existing metabolic genes along with those involved in colouring and hardening the beetle’s external skin, its cuticle. “There are these pre-existing logics that the beetle has reused,” says Parker.

In experiments, Parker’s team found that either cell type alone is insufficient to provide a survival advantage. When they blocked the activity of genes that govern either solvent or toxin production, and then placed beetles in an arena full of ants, fewer survived compared with beetles with intact secretions. The loss of access to their full toxin cocktail reduced the beetles’s survival rate by about 30 per cent.

Parker suggests the solvent cells evolved first, perhaps providing oily lubricant for the beetle’s segments. This created a niche for toxin cells to evolve, enabling a new function to emerge. Natural selection then began acting on the two cell types as a unit, further refining the contributions of each to optimise the new organ, he says.

“I think this is a nice way to phrase how organs evolve: by cells creating niches for each other, and in this way allow for the evolution of functions that otherwise wouldn’t arise because they only make sense in a certain context,” says Detlev Arendt at the European Molecular Biology Laboratory in Germany.

Reference: bioRxiv, DOI: 10.1101/2021.05.13.444042