Insect wings and body wall evolved from ancient leg segments
Preprint posted on 31 January 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
Two sets of wing homologs in the crustacean, Parhyale hawaiensis
Preprint posted on 18 December 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.
Posted on: 7 February 2018 , updated on: 19 February 2018
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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?!