Insect wings and body wall evolved from ancient leg segments

Heather S Bruce, Nipam H Patel

Preprint posted on January 31, 2018 https://www.biorxiv.org/content/early/2018/01/31/244541

Article now published in Nature Ecology & Evolution at http://dx.doi.org/10.1038/s41559-020-01349-0

and

Two sets of wing homologs in the crustacean, Parhyale hawaiensis

Courtney M Clark-Hachtel, Yoshinori Tomoyasu

Preprint posted on December 18, 2017 https://www.biorxiv.org/content/early/2017/12/18/236281

Article now published in Nature Ecology & Evolution at http://dx.doi.org/10.1038/s41559-020-1257-8

How did insects get their wings? Two preprints use CRISPR/Cas9 knockdown approaches in a crustacean to shed light on this hitherto controversial question.

Selected by Erik Clark

Categories: developmental biology, evolutionary biology, genetics

Background

The invention of insect flight 350 million years ago was momentous for the history of life on earth. However, the evolutionary origin of insect wings has been debated, unresolved, for over a century. Were they outgrowths of the insect body wall, were they exaptations of crustacean “epipods” (projections from proximal leg segments, including structures such as gills), or were they formed from a merger of the two?

Model organism studies don’t help us much, because the way that Drosophila makes its wings (from imaginal discs) is extremely derived. In recent years, however, studies in other insects have lent strong support to the “dual origin” hypothesis: in segments lacking wings, two separate tissues (the dorsal body wall and the pleural plates) express “wing” genes, and both contribute to ectopic wings formed in Hox gene knockdowns. However, it still hasn’t been clear whether these tissues ancestrally expressed wing genes, or simply co-opted them.

Key findings

Now, a pair of CRISPR/Cas9 studies in the amphipod crustacean, Paryhale hawaiensis, provide us with some clear-cut answers. Clark-Hachtel and Tomoyasu show that wing genes are necessary for the development of the dorsal body wall and epipods in Parhyale, demonstrating that the presence of a “wing” gene regulatory network (GRN) in these structures long predates the evolution of wings themselves.

In turn, Bruce and Patel knock down a number of leg patterning genes and show not only that the most proximal epipod in Parhyale is homologous to the insect pleural plate, but also that the dorsal “body wall” of both Parhyale and insects is actually a cryptic proximal leg segment, still present in other groups of crustaceans. Therefore, the two tissues from which wings develop in insects are both derived from crustacean epipods, and their shared gene expression results not from co-option, but from their common inheritance of an ancestral “epipod” GRN.

My take

This proposal offers an elegant solution to the wing origin debate, accounting for much of the evidence in favour of each of the three rival hypotheses. I also appreciated the accessibility of the text, which sidesteps much of the confusing morphological jargon of the insect/crustacean fields in favour of simple, colour-coded diagrams, allowing an outsider like me to follow the arguments. Of course, much more work will be required before we will understand how and why recognisable wings evolved within hexapods from these proto-structures. But as to the sticky question of their homology – case closed?

Related Research

Linz DM, Tomoyasu Y. (2018) Dual evolutionary origin of insect wings supported by an investigation of the abdominal wing serial homologs in Tribolium. PNAS 115, E658-E667.

Prokob J, Pecharova M, Nel A, Hornschemeyer T, Krzeminska E, Krzeminski W, Engel MS. (2017). Paleozoic nymphal wing pads support dual model of insect wing origins. Current Biology, 27, 263-269.

Martin A, Serano JM, Jarvis E, Bruce HS, Wang J, Ray S, Barker CA, O’Connell LC, Patel NH. (2015). CRISPR/Cas9 mutagenesis reveals versatile roles of Hox genes in crustacean limb specification and evolution. Current Biology 26, 14-26.

Tags: evo-devo, evolution

Posted on: 7th February 2018 , updated on: 19th February 2018

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Authors' response

Yoshi Tomoyasu and Courtney Clark-Hachtel shared about Two sets of wing homologs in the crustacean, Parhyale hawaiensis

Yoshi on the significance of the findings:

“The two studies complement each other, and together I believe that they tell an intriguing story about how complex novel structures evolve, which will no doubt significantly influence the future direction of the debates on the origin of insect wings, as well as on the evolution of morphological novelty in general.”

Courtney’s “behind the paper” story:

“One of my favorite moments from this project was the first time that I observed a ‘wingless crustacean’. When I saw that both dorsal body wall and proximal leg tissues were affected by wing gene knock-out in Parhyale and realized that this seemed to support what we had been seeing in wingless segments of insects, I got so excited. As scientists, we live for these eureka moments that can be few and far between in our work, and this moment was definitely a defining eureka moment for this project.“

1 comment

4 years

Rafael Galupa

Thanks Erik! A great example of how a specific GRN has been exploited throughout evolution… And probably a good model to keep deepening our understanding of the mechanisms behind that. I wonder how easy it is to manipulate this crustacean?!

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