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 poster child for evolutionary success: around 400,000 known species – about a quarter of all described life forms – and possibly hundreds of thousands more awaiting discovery. The beauty and diversity of beetles enchanted a young Charles Darwin and were the teenage fascination of Alfred Russell Wallace, the co-discoverers of evolution by natural selection.
But why are there so many beetles? A widely held view is that beetles gained an ecological advantage by developing the elytra, the hardened shield-like structures that protect the flight wings, allowing them to live in many different niches that other insects cannot access. Another hypothesis is that beetles co-evolved with flowering plants. As these plants diversified, so did the beetles that feed on them.
Yet both ideas fall short in explaining the largest beetle group of them all – the rove beetles (Staphylinidae) with a vast radiation of more than 66,000 species – not only the largest beetle family, but the largest family in the entire animal kingdom. Rove beetles are an enigma: they appear to have abandoned the highly protective elytra and are mostly predatory rather than feeding on plants. Yet over the past 200 million years they have exploded in Earth’s biosphere, invading every conceivable terrestrial niche.
What drove this remarkable success is the focus of a new study by researchers in the laboratory of Joe Parker, assistant professor of biology and biological engineering, Chen Scholar, and director of Caltech’s Center for Evolutionary Science. Led by former postdoctoral scientist Sheila Kitchen, the study was published online in the journal on June 17 Cellpoints to the evolution of two cell types that form a chemical defense gland in the bodies of these beetles as the catalyst behind their global radiation.
In 2021, researchers in the Parker laboratory studied a gland in rove beetles called the ‘tergal gland’, a structure at the end of their flexible abdomen. The team showed how the tergal gland is made up of two unique cell types: one that makes toxic compounds called benzoquinones, and another that makes a liquid mixture (or solvent) in which the benzoquinones dissolve, creating a powerful cocktail that the beetle releases. predators.
An ant takes on a rove beetle.
Credit: Taku Shimada
In the new work, Kitchen, Parker and their collaborators assembled whole genomes from a diverse set of species spanning the rove beetle’s evolutionary tree, and analyzed the genes expressed in the gland’s two cell types. This allowed them to discover an ancient genetic toolbox that emerged more than 100 million years ago and equipped these insects with their powerful chemical defenses.
“In assembling the genomes, we were amazed at how similar the genetic architecture of the gland was across this huge group of beetles,” says Kitchen, who is now an assistant professor at Texas A&M University. ‘When we started looking at specific gene families, we found hundreds of old genes that had found new functions in the gland, and a small but essential set of evolutionarily new genes. These new genes were crucial to the rove beetles developing their amazing properties. 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 evolution of the glands, the team identified a key evolutionary innovation in how the beetles evolved to safely produce the toxic benzoquinones. They found that rove beetles encountered a mechanism of toxin secretion that is strikingly similar to the way plants control the release of chemical compounds that deter herbivores. They bind the poison to a sugar molecule, making it inactive, and then split the poison from the sugar only when the chemical is safely excreted outside the beetle’s own cells.
“It’s quite remarkable that chemically protected beetles have stitched together virtually the same cellular mechanism as plants to avoid poisoning themselves with their own nasty chemicals,” says Parker.
This mechanism evolved in the Early Cretaceous; after evolving it, the beetles began to radiate into tens or possibly hundreds of thousands of species. “It’s the archetypal key innovation. Once they stumbled upon this solution, they really found themselves in a different place evolutionarily,” Parker says. Related rove beetles that lack the gland have not experienced the same evolutionary diversification and number only tens to hundreds of species.
By examining the chemistry of different species, the researchers found that although the two cell types that make up the gland have remained largely the same, the chemicals they produce can evolve dramatically, allowing rove beetles to adapt to different ecological niches. The gland can be thought of as a kind of chemical laboratory in which a beetle species can synthesize the compounds needed to live in new environments. For example, a group of rove beetles evolved to hunt mites and repurposed the gland to secrete mite sex pheromones; another lives in ant colonies and produces chemicals that calm the otherwise very aggressive worker ants, allowing the beetle to live symbiotically with the ants and even hunt them.
“The tergal gland of the rove beetle is an incredible, reprogrammable device for making new chemistry and developing new interactions,” says Parker. “It allowed these beetles to achieve extreme forms of ecological specialization. Without the gland, it would not have been possible to get into the weird and wonderful niches that these beetles found on their own.”
Ironically, the team found that in one beetle group the gland was redundant. According to Kitchen, “Once you’ve lived long enough in an army ant colony of millions of aggressive ants, you no longer need the gland. We found that beetles that managed to trick ants into accepting them into their societies had lost the gland their glands during evolution. Their gland toolkit genes had accumulated many inactivating mutations. An ant colony is a terrifying place for most species, but for these beetles it is a danger-free fortress instead;
The 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 predilection for beetles.
The article is titled “The genomic and cellular basis of biosynthetic innovation in rove beetles.” In addition to Kitchen and Parker, Caltech co-authors are graduate students Thomas Naragon, Jean Badroos, Joani Viliunas, Yuriko Kishi, and Julian Wagner (PhD ’24); former postdoctoral researcher Adrian Brückner; electron microscopy scientist Mark Ladinsky; former students Sofia Quinodoz (PhD ’20) and David Miller (PhD ’22); former laboratory manager Mina Yousefelahiyeh; Director of the Caltech Genomics Facility Igor Antoshechkin; and biology professor Mitch Guttman. Other 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, the Life Sciences Research Foundation, the National Science Foundation, the National Institutes of Health, the Shurl and Kay Curci Foundation, Rita Allen Foundation Scholarship, Pew Biomedical Scholarship, Alfred P. Sloan Fellowship, Iridian Genomes, Caltech’s Millard and Muriel Jacobs Genetics and Genomics Laboratory, and the American Museum of Natural History. Parker is an affiliate faculty member at Caltech’s Tianqiao and Chrissy Chen Institute for Neuroscience.