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Beetle glands help explain how complex organs evolved

Complex organs in our own bodies are composed of numerous different types of cells and tissues, all working together cooperatively to achieve a particular function. For example, a heart contains muscle tissue, valves, ligaments and nerves, all of which act to pump blood efficiently. The question is, how did these different types of tissues originally come together to work as an organ?

This question has puzzled evolutionary biologists for decades. Now it seems that new research on a species of rove beetle may be able to cast some light on the issue. Published today in the journal Cell, the research shows how two different types of cells form a specialized gland in the beetle’s abdomen, with the function of making and secreting noxious chemicals for defense. 

Rove beetles live in the leaf litter and soil of ecosystems all over the world and use cocktails of unpleasant chemical substances to keep would-be predators at bay. The beetles smear themselves and other, threatening insects, with the secreted compounds, which have the effect of triggering pain receptors in the recipient. In this way, some species of rove beetles are even able to live inside ant colonies without suffering any negative consequences.

“These beetles are fantastic models for understanding how new kinds of ecological relationships emerge during evolution, through changes at the molecular, cellular, and behavioral levels,” says senior author Joseph Parker of the California Institute of Technology. 

“As part of this question, we’re very interested in how rove beetles have pieced together these glandular structures in their abdomens, which are made of different cell types that work together. These structures are the embodiment of a major conundrum: how complex organs evolve that are often composed of many different cell types that appear to seamlessly cooperate with each other. How this cooperativity emerges during evolution is challenging to explain.”

Parker and his colleagues focused their research on Dalotia coriaria, a species of rove beetle that synthesizes and releases a defensive chemical from tergal glands in its abdomen. The substance is composed of two different types of compounds: benzoquinones, which are highly toxic solids, and solvents that consist of a blend of an alkane and esters. The solvents, on their own, are harmless, but when they dissolve the benzoquinones, they turn the resultant cocktail into a serious weapon.

Each tergal gland contains two types of cells engaged in synthesizing the different compounds to be used in defense. “One cell type makes the benzoquinones and the other makes the solvents,” Parker explains. “Both are needed to create a functional secretion that confers adaptive value.”

In the study, the investigators used single-cell transcriptomics to uncover novel enzyme pathways that are used in the creation of these substances in each cell type. They then used these findings to dig deeper, exploring how each cell type’s pathway was constructed from pre-existing components that functioned in other, more ancient cell types, elsewhere in the beetle. 

“We were able to discover the biosynthetic pathways in each cell type and could then ask how these pathways were stitched together during evolution,” noted Parker. 

Interestingly, one of the cell types – the solvent cells that make the alkane and esters – was found to be a hybrid of cuticle cells and other ancient metabolic cells used originally to make pheromones and to produce and store fats. The solvent cells now carry out their function using a mixture of enzymes from each of the ancient parental cell types. 

“The beetle has recruited a major gene expression program from these ancient metabolic cell types and installed it into a patch of cuticle, creating a gland,” said Parker.

Further experimental work with the beetles showed that, when the metabolic pathway for the production of either the solvent or the benzoquinones was rendered non-functional (by genetic knockdown), the beetles lost their defensive capabilities. 

Since both pathways are needed for the beetles’ chemical defense system, they would both have been under the influence of natural selection during the beetles’ evolutionary history. Thus, the researchers propose that the evolution of each cell type was shaped by coevolution between the two cell types. 

“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 massively raised the gland’s adaptive value, locking the two cell types into a unit where they cooperate. In essence, a new organ emerged,” said Parker.

According to the researchers, their findings illustrate how cooperation between cell types arises, generating new, organ-level behaviors. This new understanding has implications for mapping out the evolution of more sophisticated organs found across the animal kingdom, including in humans.

“Across the animal tree of life, you see complex multicellular organs that are composed of many different cell types functioning collectively,” said Parker. “Think of something like the mammalian eye, which has about 70 different cell types all functioning together to enable our visual system. The scenario we find playing out in the tergal gland – an organ made of only two cell types – you can imagine could go through further rounds as cell types create niches for new ones to be added, eventually generating really elaborate, multicellular complexity.”

By Alison Bosman, Staff Writer

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