Solving a mystery that has perplexed biologists for over a century

Injection of CRISPR solution into embryos of crustaceans (Parhyale hawaiiensis). Credit: Heather Bruce

It sounds like a “Just So Story” – “How the Insect Got its Wings” – but it is truly a mystery that has puzzled biologists for over a century. Intriguing and conflicting theories about the evolution of insect wings have emerged in recent years, but none have been entirely satisfactory. Finally, a team from the Marine Biological Laboratory (MBL), Woods Hole, resolved the controversy, using clues from long-ago scientific papers and cutting-edge genomic approaches. The study, led by MBL Research Associate Heather Bruce and MBL Director Nipam Patel, was published this week in Nature, ecology and evolution.

Insect wings, the team confirmed, evolved from a growth or ‘lobe’ on the legs of an ancestral crustacean (yes, crustacean). After this marine animal moved to Earth’s home some 300 million years ago, the leg segments closest to its body were incorporated into the body wall during embryonic development, perhaps to better support its weight on earth. “The leg lobes then moved to the insect’s back and those later formed wings,” says Bruce.

The insects incorporated two ancestral leg segments of the crustaceans (labeled 7 in red and 8 in pink) into the body wall. The lobe on leg segment 8 subsequently formed the wing in insects, while this corresponding structure in crustaceans forms the tergal plate. Credit: Heather Bruce

One of the reasons it took a century to figure this out, Bruce says, is that it wasn’t appreciated until about 2010 that insects are more closely related to crustaceans within the arthropod phylum, as revealed by genetic similarities.

“Previously, based on morphology, everyone had classified insects into the myriapod group, along with millipedes and millipedes,” says Bruce. “And if you search myriapods for the origin of insect wings, you won’t find anything,” he says. ‘So the insect wings were thought of as’ new’ structures that arose in insects and did not have a corresponding structure in the ancestor, because the researchers were looking in the wrong place for the insect’s ancestor. “

“People are very excited about the idea that something like an insect’s wings may have been a new breakthrough of evolution,” says Patel. “But one of the stories that emerge from genomic comparisons is that nothing is brand new; everything came from somewhere. And you can, in fact, understand from where. “

Parhyale hawaiensis, shown here eating, has had its genome sequenced and is the most genetically tractable crustacean for biological research. Credit: Heather Bruce

Bruce caught the smell of his now reported discovery as he compared the genetic instructions for the segmented legs of a crustacean, the tiny beach jumper Parhyaleand the segmented legs of insects, including the fruit fly Drosophila and the scarab Tribolium. Using CRISPR-Cas9 gene editing, he systematically disabled five leg modeling genes shared in Parhyale and in insects, and we found that those genes corresponded to the six leg segments that are furthest from the body wall. ParhyaleHowever, he has an additional seventh leg segment near his body wall. Where did that segment go, he wondered? “And so I started digging into the literature, and I found this really old idea that was proposed in 1893, that insects had incorporated their [closest to body] leg region in the body wall, “he says.

“But I didn’t have the story wing part yet,” he says. “So I kept reading and reading, and I came across this 1980s theory that not only did insects embed their proximal leg region into the body wall, but the small lobes of the leg later moved on to the back and have formed wings. I thought, wow, my genomic and embryonic data support these old theories. “

It would have been impossible to solve this long-standing conundrum without the tools now available to probe the genomes of a myriad of organisms, including Parhyale, which the Patel laboratory has developed as the most genetically tractable research organism among crustaceans.

Reference: “Knockout of Crustacean Leg Shaping Genes Suggest that Insect Wings and Body Walls Evolved from Ancient Leg Segments” by Heather S. Bruce and Nipam H. Patel, Dec 1, 2020, Nature, ecology and evolution.
DOI: 10.1038 / s41559-020-01349-0