A beetle chemical defense gland offers clues about how complex organs
evolve

Date:
December 9, 2021
Source:
Cell Press
Summary:
Rove beetles are among the chemists of the insect world, concocting
noxious compounds within their bodies that are weaponized to ward
off predators, enabling the beetles to survive in leaf litter
and soil in ecosystems across the planet. Investigators studying
a species of rove beetle report how two distinct cell types have
come together to form a specialized gland for making and secreting
these defensive cocktails. The work has implications for mapping
out the evolution of more sophisticated organs found across the
animal kingdom, including in humans.



FULL STORY ==========================================================================
Rove beetles are among the chemists of the insect world, concocting
noxious compounds within their bodies that are weaponized to ward off predators, enabling the beetles to survive in leaf litter and soil
in ecosystems across the planet. On December 9 in the journal Cell, investigators studying a species of rove beetle report how two distinct
cell types have come together to form a specialized gland for making
and secreting these defensive cocktails. The work has implications for
mapping out the evolution of more sophisticated organs found across the
animal kingdom, including in humans.


========================================================================== "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 (@Pselaphinae) 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's lab focuses on
rove beetles in part because of their ability to carve out niches for themselves in many different ecosystems, from in the dirt to inside ant colonies. One way they've been able to survive in the presence of other insects, such as ants, is through glands in their abdomen that release
a defensive chemical compound that triggers pain receptors. The beetles
have a supremely flexible body and can smear these chemical cocktails
directly onto predators to defend themselves.

The species of rove beetle that was the focus of this research, Dalotia coriaria, has what's called a tergal gland in its abdomen that releases
a cocktail made of two compound types: benzoquinones, which are highly
toxic but solids on their own, and solvents, a fatty acid-derived blend
of an alkane and three esters. The latter compounds by themselves are
benign, but they weaponize the benzoquinones by dissolving them.

Parker's group investigated the tergal gland and found two cell types that
were engaged in a biosynthetic division of labor. "One cell type makes the benzoquinones and the other makes the solvents," Parker says. "Both are
needed to create a functional secretion that confers adaptive value."
In the study, the investigators used single-cell transcriptomics of
the beetles' abdominal segments to uncover novel enzyme pathways that
enable 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 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," Parker notes.

Remarkably, one of the cell types -- the solvent cells that make the
alkane and esters -- was found to be a hybrid of cells comprising the
beetle's exoskeleton and two ancient metabolic cell types that make
and store lipids and produce pheromones. "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," Parker says.

Further experiments -- including placing the beetles into battle arenas
with ants -- revealed that when either the solvent or benzoquinone pathway
was knocked down, the beetles lost their defensive capabilities. This
suggested that under natural selection, both cell types are needed to
confer the beetles' chemical defense system. The investigators also found
that the compound made by the tergal gland has antimicrobial properties, further raising the adaptive value of the gland.

The authors think the gland evolved via 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," Parker says.

"Across the animal tree of life, you see complex multicellular organs
that are composed of many different cell types functioning collectively," Parker concludes. "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." ========================================================================== Story Source: Materials provided by Cell_Press. Note: Content may be
edited for style and length.


========================================================================== Journal Reference:
1. Adrian Bru"ckner, Jean M. Badroos, Robert W. Learsch, Mina
Yousefelahiyeh, Sheila A. Kitchen, Joseph Parker. Evolutionary
assembly of cooperating cell types in an animal chemical defense
system. Cell, 2021; 184 (25): 6138 DOI: 10.1016/j.cell.2021.11.014 ==========================================================================

Link to news story: https://www.sciencedaily.com/releases/2021/12/211209142600.htm

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