Chinese-Led Team Solves a Century-Old Insect Wing Puzzle: Mayflies and Dragonflies Are Sisters

October 13 — According to Xinhua, an international research team led by the Nanjing Institute of Geology and Palaeontology of the Chinese Academy of Sciences and Nanjing Normal University has used phylogenomic methods to solve the “Palaeoptera problem” that has puzzled insect scientists for more than a century. The results were published today in the international journal Proceedings of the National Academy of Sciences (PNAS).

The study confirms that mayflies and dragonflies are sister groups that together make up the Palaeoptera, and that the Palaeoptera is in turn the sister lineage of the Neoptera, the insects with foldable wings.

Note: the “Palaeoptera problem” refers to the long-unresolved phylogenetic relationships among three groups of winged insects — the mayflies (Ephemeroptera), the dragonflies (Odonata) and the Neoptera, whose wings can fold.

Previously, the kinship of dragonflies, mayflies and other winged insects was disputed and was one of the hardest nodes in insect phylogeny to resolve. In this study, the team drew on China’s rich mayfly species resources, newly sequencing the nuclear genomes of 16 native mayfly species and integrating genome and transcriptome data from more than a hundred insects, filling the previous shortfall in sampling of key groups.

The results of several phylogenomic analysis methods consistently support the monophyly of the Palaeoptera — that is, mayflies and dragonflies are sister groups, and together they form the Palaeoptera, which is the sister lineage of the Neoptera. This conclusion corrects a long-standing traditional view based on morphological features. Some scholars had previously inferred that, because palaeopteran wings cannot fold and appear “more primitive,” the group must have originated earlier than the Neoptera. The new study shows instead that, after the two lineages diverged, each independently evolved different wing-base structures: the Palaeoptera specialised in a rigid wing base suited to gliding or high-speed flight, while the Neoptera evolved a foldable wing-root joint that makes it easier to move about in confined spaces.

The study also combined 13 fossil calibration points with molecular clock data to update the origin time of winged insects. The molecular clock results show that crown-group winged insects date back to the Early Devonian, about 419 million to 393 million years ago, while the palaeopteran crown group originated in the Late Devonian. Insect wings appeared only once in evolutionary history: the wings of today’s bees, butterflies and dragonflies are all inherited from the same ancient common ancestor. The Neoptera’s mechanism of folding the hindwings over the abdomen by rotating an independent third axillary plate laid the physiological and ecological foundation for the explosive radiation of the Neoptera after the Carboniferous.

According to the Nanjing Institute of Geology and Palaeontology, the study also explains why earlier research based on omics data could not solve the Palaeoptera problem: during the rapid radiation of early winged insects, incomplete lineage sorting combined with gene tree estimation error left as much as about 40% of gene trees inconsistent with the species tree, so different analysis methods produced contradictory conclusions. Using concatenation and coalescent methods, multiple evolutionary models, topology tests and gene-locus-level signal dissection, the study systematically examined the developmental signal.

Cai Chenyang, a researcher at the Nanjing Institute of Geology and Palaeontology, said that insects taking to the sky was a landmark innovation in the history of life on land: the birth of wings gave insects a whole new realm of activity and changed the face of terrestrial ecosystems. Zhou Changfa, a professor at Nanjing Normal University, said the two evolutionary paths developed in parallel and together shaped the diverse flight styles and rich species of insects today.

The paper’s first authors are Du Shiyu, a postdoctoral researcher at Nanjing Normal University, and Wang Yehao, a doctoral student at the Nanjing Institute of Geology and Palaeontology; Cai Chenyang and Zhou Changfa are the co-corresponding authors, with Michael S. Engel, a professor at the American Museum of Natural History, and others taking part in the research.