With nearly 100,000 species, the Acercaria (lice, plant lices, thrips, bugs) including number of economically important species is one of the most successful insect lineages. However, its phylogeny and evolution of mouthparts among other issues remain debatable. Here new methods of preparation permitted the comprehensive anatomical description of insect inclusions from mid-Cretaceous Burmese amber in astonishing detail. These “missing links” fossils, attributed to a new order Permopsocida, provide crucial evidence for reconstructing the phylogenetic relationships in the Acercaria, supporting its monophyly, and questioning the position of Psocodea as sister group of holometabolans in the most recent phylogenomic study. Permopsocida resolves as sister group of Thripida + Hemiptera and represents an evolutionary link documenting the transition from chewing to piercing mouthparts in relation to suction feeding. Identification of gut contents as angiosperm pollen documents an ecological role of Permopsocida as early pollen feeders with relatively unspecialized mouthparts. This group existed for 185 million years, but has never been diverse and was superseded by new pollenivorous pollinators during the Cretaceous co-evolution of insects and flowers. The key innovation of suction feeding with piercing mouthparts is identified as main event that triggered the huge post-Carboniferous radiation of hemipterans, and facilitated the spreading of pathogenic vectors.

In response to predation pressure, some insects have developed spectacular plant mimicry strategies (homomorphy), involving important changes in their morphology. The fossil record of plant mimicry provides clues to the importance of predation pressure in the deep past. Surprisingly, to date, the oldest confirmed records of insect leaf mimicry are Mesozoic. Here we document a crucial step in the story of adaptive responses to predation by describing a leaf-mimicking katydid from the Middle Permian. Our morphometric analysis demonstrates that leaf-mimicking wings of katydids can be morphologically characterized in a non-arbitrary manner and shows that the new genus and speciesPermotettigonia gallicadeveloped a mimicking pattern of forewings very similar to those of the modern leaf-like katydids. Our finding suggests that predation pressure was already high enough during the Permian to favour investment in leaf mimicry.

When the same complex trait is exhibited by closely related species, a single evolutionary origin is frequently invoked. The complex stridulatory apparatus present in the forewings of extant crickets, mole crickets, katydids, and prophalangopsids, is currently interpreted as sharing a single common origin due to their similarity and unique function. An alternative hypothesis of convergent evolution in these ensiferan groups has challenged this common view, but remained controversial because of competing interpretations of wing venation. Here we propose another hypothesis for the widely and long debated homology of ensiferan stridulatory apparatus, performing the first 3D reconstruction of hidden structures at the wing bases. This approach allowed defining the homology of each vein from its very origin rather than after its more distal characteristics, which may be subjected to environmental pressure of selection. The stridulatory apparatus involves different veins in these four singing clades. In light of the most recent phylogenetic evidence, this apparatus developed four times in Ensifera, illustrating extraordinary convergent evolutions between closely related clades, by far exceeding the number of evolutionary steps ever proposed for calling ability in this group.