As organisms on planet Earth diversified, some branches of the tree of life became exceptionally diverse, others much less so. Still others became extinct. Why evolution favored certain groups over others is a long-standing question in evolutionary science.
Beetles are the children of evolutionary success: about 400,000 species are known—about a quarter of all described life forms—and potentially hundreds of thousands more await discovery. The beauty and diversity of beetles enchanted the young Charles Darwin and fascinated teenage Alfred Russell Wallace, the co-discoverer of evolution by natural selection.
But why are there so many bugs? One widely held view is that the beetles gained an ecological advantage by developing elytra, the hardened shield-like structures that protect the flight wings, allowing them to live in many different niches that other insects cannot reach. Another hypothesis is that beetles co-evolved with flowering plants. As these plants diversified, so did the bugs that feed on them.
Yet both of these ideas fall short in explaining the largest group of beetles of all—the Staphylinidae, a vast radiation of more than 66,000 species—not only the largest family of beetles, but the largest family in the entire animal kingdom. Rove beetles are an enigma: they both appear to have abandoned the heavily protective elytra and are mostly carnivorous rather than feeding on plants. Yet they have exploded across Earth’s biosphere, invading every terrestrial niche imaginable over the past 200 million years.
The reason for this remarkable achievement is the focus of a new study by researchers in the lab of Joe Parker, an assistant professor of biology and biological engineering, a Chen Scholar and director of Caltech’s Center for Evolutionary Science. The study, led by former postdoctoral fellow Sheila Kitchen, appeared online June 17 in the journal Cellshows the development of two types of cells that form a chemical defense gland in the bodies of these beetles as a catalyst for their global radiation.
In 2021, researchers in Parker’s lab studied a gland in rove beetles called the “tergal gland,” a structure at the tip of their flexible abdomen. The team showed how the tergal gland consists of two unique types of cells: one makes toxic compounds called benzoquinones, and the other makes a liquid mixture (or solvent) in which the benzoquinones dissolve, creating a potent cocktail that the beetle unleashes on a predator.
The little ant is facing the little ant.
Credit: Taku Shimada
In the new work, Kitchen, Parker and their collaborators assembled the whole genomes of a diverse set of species spanning the raptor evolutionary tree and analyzed the genes expressed by the gland’s two cell types. This allowed them to uncover an ancient genetic toolkit that evolved more than 100 million years ago, equipping these insects with their powerful chemical defenses.
“As we assembled the genomes, we were struck by how similar the genetic architecture of the gland was across this massive group of beetles,” says Kitchen, who is now an assistant professor at Texas A&M University. “It was when we started looking at specific gene families that we found hundreds of ancient genes that found new functions in the gland, and a small but essential set of evolutionarily new genes. These new genes were the key to the vagrants developing their amazing chemistry Telling this story was made possible by our fantastic interdisciplinary team of evolutionary biologists, chemical ecologists, protein biochemists and microscopists.”
By tracing the molecular steps in the development of the gland, the team identified a major evolutionary innovation in the way the beetles evolved to safely produce the poisonous benzoquinones. They found that the rove beetles have hit on a toxin secretion mechanism that is strikingly similar to how plants control the release of chemical compounds that repel herbivores. They bind the toxin to a sugar molecule, rendering it inactive, and then only cleave the toxin from the sugar when the chemical is safely excreted outside the bug’s own cells.
“It’s quite remarkable that chemically protected bugs have put together essentially the same cellular mechanism as plants to avoid being poisoned by their own nasty chemicals,” says Parker.
This mechanism evolved in the early Cretaceous; after they developed it, the beetles began to radiate into tens or perhaps hundreds of thousands of species. “It’s the archetypal key innovation. Once they hit on that solution, it really took off, evolutionarily speaking,” says Parker. Related lineages of raptors that lack the gland have not had the same evolutionary diversification, numbering only tens to hundreds of species.
By examining the chemistry of different species, the researchers remarkably found that while the two types of cells that make up the gland have remained largely the same, the chemicals they produce can evolve dramatically, adapting the beetles to different ecological niches. The gland can be considered a kind of chemical laboratory in which the beetle species can synthesize the compounds needed to live in new environments. For example, one group of marsupials evolved to feed on mites, converting the gland’s function to secreting the mites’ sex pheromones; another lives inside ant colonies and produces chemicals that calm the otherwise highly aggressive worker ants, allowing the beetle to live symbiotically with the ants and even hunt them.
“The raptor’s tergal gland is this incredible, reprogrammable device for making new chemicals and developing new interactions,” says Parker. “It allowed these bugs to achieve extreme forms of ecological specialization. Without the gland, it would have been impossible to get into the weird and wonderful niches these bugs found.”
Ironically, the team found that one group of beetles had a redundant gland. According to Kitchen: “Once you’ve lived inside an army ant colony of millions of aggressive ants long enough, you no longer need the gland. We found that the beetles that managed to trick the ants into accepting them into their society lost their glands during evolution and accumulated a lot of inactivating mutations. An ant colony is a scary place for most species, but for these beetles it’s a fortress without danger – instead, they’ve got the ants to protect them.”
A new study highlights how evolutionary changes at the cellular level can have major long-term consequences for ecological and evolutionary diversification. In this case, it contributes to nature’s excessive fondness for bugs.
The paper is titled “The Genomic and Cellular Basis of Biosynthetic Innovation in Rove Beetles.” In addition to Kitchen and Parker, the co-authors are Caltech graduate students Thomas Naragon, Jean Badroos, Joani Viliunas, Yuriko Kishi, and Julian Wagner (PhD ’24); former postdoc Adrian Brückner; electron microscopy scientist Mark Ladinsky; former graduate students Sofia Quinodoz (PhD ’20) and David Miller (PhD ’22); former laboratory head Mina Yousefelahiyeh; Caltech Genomics Facility Director Igor Antoshechkin; and biology professor Mitch Guttman. Additional co-authors include K. Taro Eldredge of the University of Michigan, Stacy Pirro of Iridian Genomes, Steven Davis of the American Museum of Natural History, and Matthew Aardema of Montclair State University.
Funding was provided by Caltech’s Center for Evolutionary Science, Life Sciences Research Foundation, National Science Foundation, National Institutes of Health, Shurl and Kay Curci Foundation, Rita Allen Foundation Scholarship, Pew Biomedical Scholarship, Alfred P. Sloan Fellowship, Iridian Genomes, Caltech’s Millard Laboratory and Muriel Jacobs Genetics and Genomics Laboratory and American Museum of Natural History. Parker is an associate faculty member with the Tianqiao and Chrissy Chen Institute for Neuroscience at Caltech.