When a theologian asked J.B.S. Haldane what he could infer about the mind of God from studying the natural world, the famed evolutionary biologist was said to have replied, “God has an inordinate fondness for beetles.”
That quotation is perhaps apocryphal but also contains a large grain of truth. The evidence comes from the more than 400,000 species of beetles belonging to 190 families that have been described so far. That means that about one quarter of all 1.5 million species known to science (across all animals, plants and microbes) are beetles. In fact, the group’s vast diversity “was probably one of the things that led [Charles] Darwin and [Alfred Russel] Wallace to hatch on the mechanism of natural selection,” explains Max Barclay, senior curator of beetles at the Natural History Museum in London. “So we think the diversity of beetles actually has contributed to our understanding of our place in the universe. But since then a lot of scientists have been trying to figure out the reason for this remarkable diversity.”
One early idea that was proposed as an explanation is that beetles have hardened forewings, called elytra, that form a protective capsule over their flight wings. This allows them to live in all kinds of environments that insects with unprotected wings can’t get into—underneath tree bark, inside mammal dung or in birds’ nests, to name a few. Another idea that has been proposed is that plant-eating beetles diversified along with land plants as the plants themselves split into many lineages over evolutionary time. As the beetles specialized to feed on a particular plant, they would have split into different species.
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But the very biggest family of beetles continued to defy explanation because their elytra are highly reduced, and they don’t feed on plants. This family, the “monster in the room,” comprising more than 66,000 species, is the Staphylinidae. Also known as rove beetles, the Staphylinidae family “is not just the biggest family in the beetles; it’s the biggest family in the entire animal kingdom,” says Joe Parker, an evolutionary biologist at the California Institute of Technology.
In appearance, rove beetles are small and drab insects that eat critters in leaf litter. They don’t come from a particularly impressive evolutionary stock, and there’s nothing especially remarkable about them. So how did they become the poster child for evolutionary success? “Something happens along this one particular rove beetle lineage called the Aleocharinae that explodes in diversity. And what is that thing? They all have this incredible chemical defense gland in the abdomen,” Parker says.
Aleocharinae, with about 17,000 known species, is the largest subfamily within the Staphylinidae family. Parker suspects it’s only the “tip of the iceberg”—there are probably hundreds of thousands of species in this relatively poorly studied group.
A secret of Aleocharine beetles’ success may now have been found. Parker and his team have figured out how and when the chemical defense gland in these rove beetles’ abdomen evolved—and why it was the key to this lineage’s subsequent evolutionary flourishing. The findings from Parker’s research team were posted to the bioRxiv preprint server in May and are under review in a journal for publication.
The chemical defense gland is extremely useful because it allows the beetles to repel and deter predators that would eat them. “Having an adaptive advantage is not a reason for being species-rich,” however, points out Alfried Vogler, who studies beetles at Imperial College London and was not involved in this research.
Something else had to drive that diversification. “The question is, why would small predators in the leaf litter become so diverse?” Barclay asks. “It’s difficult to think of a reason for that because what they’re doing is really quite straightforward. They’re hunting down larvae of other insects or worms or slugs and eating them.”
One idea is that ants, fearsome predators that first appeared in the fossil record about 100 million years ago, probably drove the evolution and diversification of rove beetles, Parker suggests. It is difficult, he says, to overestimate just how much ants have shaped modern terrestrial ecosystems by driving many insect species to extinction, especially in the last 50 million years. He argues that the rove beetles have survived and succeeded because they've found various chemical strategies to defend against ants—and live alongside them, sometimes even inside their nests.
In the new study, Parker’s team sequenced the genomes of several rove beetle species and their relatives to piece together the timing and sequence of the evolution of the chemical defense gland. They found that the gland first evolved about 148 million years ago, at the boundary of the Jurassic and Cretaceous periods. But at that time, the gland only made a fatty acid solvent similar to the hydrocarbons that almost all insects make in their cuticles to prevent desiccation and to communicate chemically. It wasn’t until later, about 110 million years ago, that the beetles’ ability to make toxic chemicals that activate pain receptors evolved. In fact, the gland required the evolution of two new cell types: one that makes a harmless fatty acid solvent and another that makes a toxic cocktail of compounds called benzoquinones. The benzoquinones need to be dissolved in the fatty acid solvent to become a potent mixture that beetles can spray on attacking ants to repel them.
The researchers found that this gland has been conserved in thousands of rove beetle species over eons because it is so effective at protecting against ants. At the same time, it has also been the foundation for all kinds of chemical innovation. A few rove beetle species that feed on mites have evolved glands that are not toxin-producing but instead emit a chemical that mimics the sex pheromones (mating chemicals) of mites in order to lure—and eat—them.
Other lineages of rove beetles have integrated themselves into ant colonies. Called myrmecophiles (“ant lovers”), these beetles make chemicals that pacify ants rather than repel them. The beetles also collect hydrocarbons from the ants’ cuticle in order to smear themselves with the chemical signature specific to each ant nest. This allows them to disguise themselves as ants and to live and thrive within the ant nests, where they find a constant source of food and protection. These are just some of the various ways that chemical innovations have allowed rove beetles to thrive. “The chemical deceit is very sophisticated,” Barclay says. “Basically, a general-purpose weapon has been refined to all kinds of additional uses.”
Parker’s team also figured out a clever way that the rove beetles avoid poisoning themselves with the dangerous benzoquinones. They keep the chemical precursor of the toxin separate from the enzyme that catalyzes the last step of the reaction to produce the toxin. By holding these two chemicals in separate cellular compartments, the benzoquinone-producing cells ensure the toxic stuff isn’t produced internally within the cells. Only when the precursor and the enzyme are released together outside of the cell is the toxin formed. When the toxin is released in the gland, which is on the outside of the body, it is then dissolved in the solvent, and it can be sprayed onto any attacking ants.
Interestingly, this isn’t the first time the natural world came upon this clever solution for handling poisons safely. This two-compartment strategy is also commonly found in plants that make toxins to repel herbivores from eating them.
Thus, the unassuming rove beetles succeeded by becoming virtuosos of chemistry, and they have converged on some of the same tricks that other lineages in the living world discovered independently to handle poisons safely.
Critically, the chemical defense gland in beetles existed for tens of millions of years before ants became an ecological force to be reckoned with. It was only after ants started to proliferate in terrestrial ecosystems in the last 50 million years that they drove many invertebrate species to extinction, which led to selection for lineages that could coexist with ants thanks to chemical or physical defenses. “The key thing is that certain traits have evolved for a long time but suddenly take on a newfound relevance for lineage diversification” when something in their environment changes, Parker says.
Still, Barclay thinks the ants may only be a partial explanation for the rove beetles’ diversity. When plants drove the diversification of plant-eating beetles, the number of new beetle lineages was more or less in proportion to the number of new plant species. But the rove beetles are much, much more diverse than the ants. So there’s got to be something else, Barclay says.
In the end, it’s clear that there’s no single, sweeping reason for beetles’ incalculable diversity, but rather a variety of factors that each contribute to their success. That’s what makes it “a kind of frustrating question because it doesn’t, so far, have a straightforward answer,” Barclay says. “So it’s quite brave to even attempt it.”