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Abstract
The vast diversity in morphology of insect wings provides an excellent model to study
morphological evolution. The best-described wing modification is the specification
of halteres in Drosophila by a Hox-dependent mechanism, in which a Hox gene affects
the expression of genes important for wing development to modify the resulting structure.
We have previously shown that highly modified beetle elytra are Hox-free structures
despite their divergent morphology, suggesting another mode of evolutionary modification.
To understand how elytra have evolved without Hox input, we have analyzed wing development
in a coleopteran, Tribolium castaneum. Based on Drosophila mutant phenotypes, we first
hypothesized that changes in the wing gene network might have contributed to elytral
evolution. However, we found that the wing gene network defined in Drosophila is largely
conserved in Tribolium and is also used to pattern the elytra. Instead, we found evidence
that the exoskeleton formation has been co-opted downstream of the conserved wing
gene network multiple times. We also show evidence that one of these co-options happened
prior to the others, suggesting that repeated co-options may have strengthened an
advantageous trait. In addition, we found that the Tribolium apterous genes are not
only essential for exoskeletalization of the elytra but also are required for the
proper identity of the hindwing-an unexpected role that we find to be conserved in
Drosophila.
Our findings suggest that elytral evolution has been achieved by co-opting a beneficial
trait several times while conserving the main framework of wing patterning genes.