Thread by @Pselaphinae

Beetles are the archetype of biological diversity: ~1/4 of described lifeforms are beetles.
Why this "inordinate fondness" is one of evolutionary biology's enduring questions. We connect it to evolution deep down at the cellular level:
biorxiv.org/content/10.110…

This study was headed by the remarkable @Dr_SKitch while a postdoc in our lab. Key contributions from @NaragonTom @AdrianBrueckner @sofiquinodoz @JoaniViliunas @JMyrmecoWagner @DavidMillerP @mitchguttman @MatthewAardema +others not on twitter. Congrats Sheila (and everyone else)!

So, why so many beetles? If there's one "key innovation" that almost all beetles have it's elytra — the hardened forewings that protect the delicate flight wings.

Elytra enable beetles to access parts of ecosystems that are shut off to insects with unprotected wings: soil/litter/under bark/dead wood/internal parts of plants/vertebrate nests...the list is endless. Plus, beetles can still fly>disperse>speciate. Cue 400,000 beetle species?

Possibly, but the beetle phylogeny is profoundly unbalanced. >50% of species are clustered into just 5/190 beetle families. Additional lineage-specific factors must have shaped beetle cladogenesis. Understanding these historical contingencies is key to explaining beetle diversity

One explanation for the huge diversity of certain beetle groups is phytophagy (plant feeding). Switching from gymnosperms/cycads to feeding on radiating angiosperms (flowering plants) may have catalyzed diversification of some of the biggest beetle clades
science.org/doi/10.1126/sc…

Phytophagy was itself contingent on innovations in metabolism: acquisition of plant cell wall-degrading enzymes, and endosymbiotic bacteria. These allow phytophagans to digest plant material, unlocking recalcitrant nutrients, eg:
pnas.org/doi/abs/10.107…
sciencedirect.com/science/articl…

Beetle-angiosperm co-diversification is a powerful explanation... but only up to a point. Because ~2/3 of beetles are not phytophagous. Great discussion of the model's limitations by @Coleopterist and @TimBarraclough9 here:
sciencedirect.com/science/articl…

In fact, there is a real monster in the room in the form of the single biggest family, both in the Coleoptera and within the entire Metazoa.
These beetles aren't phytophagous, and don't even fit the typical beetle body plan.

They are the rove beetles (Staphylinidae)—a clade of >66,000 described species. That's about the same size as the entire vertebrate subphylum. Its true diversity is several-fold greater.
sciencedirect.com/science/articl…

Rove beetles have reconfigured the beetle body plan: the elytra are short, exposing an elongate, flexible abdomen. This anatomy enables them to move rapidly (undulate) through substrates, chasing down prey. So, a massive, largely predatory clade. Why SO MANY of them?

Well, again, diversity is not evenly spread across rove beetles. Most species are clustered into one subfamily—the Aleocharinae—a clade of 16,837 known species: the biggest animal subfamily. Tens of thousands more are undescribed. This one group is the Mount Everest of beetles...

Aleocharinae is not only numerically massive, but might be the most ecologically diverse beetle clade. These tiny (2-6mm) predators have proliferated globally throughout tropical+temperate soil/leaf litter. Poke any patch of dirt and you'll find them....

They've reached extremes on subantarctic islands, caves/deep soil/intertidal zones... even transiently submerged coral reefs. They've undergone remarkable specialization: clades of ectoparasitoids, vertebrate commensals, fungus/dead wood/plant-feeders...

(yes, they've even evolved phytophagy just for kicks 😂)

Most dramatically, they've repeatedly departed a free-living lifestyle, transforming into symbionts of colonies of ants (myrmecophiles) and termites (termitophiles), evolving remarkable behaviors/chemistries/anatomies to infiltrate insect societies
sciencedirect.com/science/articl…

So, what's so special about these minuscule beetles that's enabled them to explode in diversity, and adapt to countless ecological niches?

It seems like a paradox: when rove beetles evolved their flexible bodies, they sacrificed physical protection of the abdomen, forsaking a bit of their beetle identity...

And yet this one lineage, Aleocharinae, went on to become a global beetle superpower...

The key, perhaps, was chemistry.

Exposing the flexible abdomen opened the door for a new mode of innovation. The beetles evolved defense glands, accurately targetable at other organisms.

This massive family became the chemists of the insect world.
sciencedirect.com/science/articl…

Aleocharines have been amongst the most accomplished of the rove beetle chemists. These beetles possess a unique "tergal gland" on the dorsal abdomen. The chemistry in this gland packs a punch...

The "business" compounds in this secretion are benzoquinones: irritants that activate TRPA1 channels (pain receptors). But the benzoquinones are solid compounds, useless on their own...

But evolution devised a brilliant trick. The gland comprises two cell types: one making benzoquinones (the "BQ cells"), another making an alkane/ester solvent into which they dissolve (the "solvent cells").

Solvent cells form a chemical reservoir inside the beetle's abdomen, into which both cell types secrete. Combining the compounds to create a cocktail in this way unlocks the benzoquinones' toxicity, weaponizing the total secretion.

We previously showed how these unique cell types coevolved with each other to create this cooperative, organ-level system. This process involved repurposing ancestral enzyme pathways and transcriptional programs from the beetle's primary metabolism.
cell.com/cell/fulltext/…

A thread about this earlier work is here:

https://twitter.com/Pselaphinae/status/1394747693763727363

Stitching together this new organ seems to have been a big deal macroevolutionarily. Aleocharinae exploded throughout modern ecosystems, invading even the most predator-dense habitats (ant-dominated litter/ social insect colonies).

The gland bought aleocharines enemy-free-space throughout the terrestrial biosphere. Its secretion also has strong antimicrobial effects, which might also have helped them colonize new niches via pathogen suppression.

The tergal gland is a feature unique to almost all aleocharines, but not all....
The earliest-branching lineages missed out on the gland: they are far more species-poor, with limited ecological diversity. Same is true of closely-related outgroup subfamilies that lack the gland.

So, getting back to the question of historical contingencies in explaining the pattern of beetle diversification...

Some really important events happened along lineage leading to the clade that eventually got this gland—the so called "Higher Aleocharinae".

(Time to pick the kids up from summer camp 😄) …tbc