The forewing of Permotettigonia is very broad compared with its length, only ca. 2.7 times longer than wide, with its surface separated into two main fields of nearly the same width (subcostal field and field between R and CuA of the same width, both 6.0 mm wide), separated by a pair of parallel longitudinal strongly marked veins ScP and R, secondary veinlets in subcostal and median fields nearly perpendicular to main veins, with those of subcostal field emerging obliquely from ScP and making a strong bend just after their base, and subcostal field corrugated. The presence of a pronounced angle between the anal field and the rest of the tegmen suggests that the tegmina of Permotettigonia were not held horizontally but perpendicular to the body. All these structures mirror those of some modern leaf-like macropterous Tettigoniidae14 that have an appearance of upright leaves (case of occultation of the volume as relief, surface and outline), for example, Pterophylla15,16, suggesting a similar situation for Permotettigonia.

To examine the possibility that the tegmina of Permotettigonia could display a leaf-mimicking camouflage, we compared it with morphometric descriptors distinctive of the modern leaf-mimicking katydids. As such morphometric descriptors were not already available; we performed a comprehensive morphological analysis of the tegmina of modern katydids (data set in Supplementary Table 1). Pterochrozinae is the only tettigoniid subfamily including only leaf-mimicking species17,18, which are considered the most perfectly camouflaged katydids. This subfamily was therefore used to epitomize leaf-mimicking species.

We carried out morphometric analyses in a set of representative modern tettigoniids, including Pterochrozinae and other subfamilies with univariate (non-linear regression and curve-fitting), bivariate (correlation between variables) and multivariate (Principal Component Analysis or PCA) approaches, based on size-independent measures (ratios) to focus on shape analysis.

These analyses allowed to distinguish significantly two wing morphologies (Fig. 2; Supplementary Figs 3–8): one is corresponding to the tegmina of genera known for displaying leaf mimicry (including Pterochrozinae), and the second to the non-mimetic tegmina. Distributions of morphological descriptors were significantly better fitted with two components models having one component fixed to values obtained from Pterochrozinae, than with one-component models (Supplementary Table 2). For all parameters, treated with non-linear regression models and curve-fitting, that allow modern leaf-mimicking species to be distinguished from other katydids, Permotettigonia displayed values shared by at most 3% of the modern non-leaf-mimicking species and by up to 30% of modern leaf-mimicking species (Fig. 2a,b, Supplementary Table 3, Supplementary Figs 3–6).As the radial vein is strongly zigzagged and not thickened in Archepseudophylla, parameters involving this vein are not relevant to analyse this taxon. Both the circularity and the ratio width/length, which do not involve the radial vein, confirm that this fossil is close to the morphology of extant mimetic species, but relatively less than the Permian fossil. In the morphospace of tettigoniid tegmina using PCA, it is very close to Permotettigonia inside the mimetic group as defined by Mugleston et al.14 (Fig. 2c).

Figure 2: Morphometric analyses of leaf-mimicking versus non-leaf-mimicking tegmina. (a,b) Non-linear regression modeling. (a) Tegmina width/length ratio. (b) Anterior field area/posterior field area ratio. (c) Morphospace of tettigoniid tegmina using PCA, Ordination of 253 modern Tettigoniidae, the Cenozoic Archepseudophylla fossilis Nel et al., 2008, plus Permotettigonia gallica, based on five morphometric indices defined in Supplementary Information. Taxa plotted in a factorial map divided into two confidence ellipses using Mugleston et al.14 criterion, nM centroid of cloud of non-mimetic taxa, M centroid of cloud of mimetic taxa. F Permotettigonia gallica. Values for Permotettigonia are indicated by grey triangles, and white triangle for Archepseudophylla. Full size image

Using PCA that allows visualizing the set of all variables in the same space (or morphospace analysis), Permotettigonia is close to the centre of the set of leaf-mimicking species as defined by Mugleston et al.14 (Fig. 2c). Furthermore, if we consider a PCA based on the different subfamilies, Permotettigonia is between the Pterochrozinae and the Pseudophyllinae; two clades that mainly comprise leaf-mimicking species (see Supplementary Fig. 7).

The morphometric results strongly support the leaf mimicry function of the tegmina of Permotettigonia. The difficulty is to determine which kind of leaves Permotettigonia could have mimicked. Of course the angiosperms were not present during the Permian, but plants with very similar leaf or pseudoleaf morphology were present, symmetrical to a midvein, and with subperpendicular second order veins and marked corrugations. It is especially the case of the very large angiosperm-like leaves of the Gigantopterideae and of some other tracheophytes lineages19,20,21.

Unfortunately, no plant is recorded from the Cians Formation. However, two red Middle Permian palaeofloras of similar ages are known, from the Bau Rouge Member (Kungarian–Roadian22,23, Toulon Basin, Var), and the Mérifons Member (Kungurian–Capitanian23,24, Salagou Formation, Lodève Basin, Hérault), at ∼150 and 350 km from the Dome de Barrot. All these outcrops are corresponding to shallow playa lakes and submerged flood plains25.

In the Bau Rouge Member and the Salagou Formation, the Taeniopteris leaves (a type of plant ranging between the Late Paleozoic to the Mesozoic) are one of the best-known candidates for a mimicry by Permotettigonia because they can be up to 5 cm wide with the surface presenting a series of corrugations perpendicular to a strong midvein (Supplementary Fig. 10), quite similar to the corrugations of the wing of Permotettigonia26. Also, the second-order veins of the leaves of Taeniopteris are separating obliquely from the main midvein and becoming more or less perpendicular to the margin, quite similarly to the veinlets in the subcostal field of Permotettigonia. The other possible problem is the length of the leaf (up to 22 cm long). Nonetheless, some modern katydids can be mimetic with leaves that are substantially longer than the insect, for example, Segestidea living on Calamus palms27. Moreover, the leaves of Taeniopteris were also attacked by insects in the Permian, having margin feedings attributed to orthopteroid insects20,28,29,30.

Permotettigonia may have been both an imitator of living plants as well as parts of leaves among which it could go unnoticed, especially if it had also a cryptic coloration (homochromy), a character that unfortunately remains unknown (see possible reconstruction in Fig. 3). It is likely that this mimicry conferred an advantage in avoiding detection by predators, such as flying insects (like giant griffenflies, also recorded from the Dôme de Barrot31) and terrestrial tetrapods.

Figure 3: Reconstruction of Permotettigonia gallica gen. et sp. nov. on Taeniopteris sp. Body interpreted after a Pterophylla sp. with the tegmen of P. gallica (copyright C. Garrouste). Full size image

During the Late Carboniferous and the Early Permian, the pressure of predation on the palaeopteran flying insects by land vertebrates was probably relatively low compared with that by carnivorous flying insects, such as giant griffenflies31. The plant–insect homomorphy is not recorded at that time and disruptive coloration was relatively rare among the neopteran insects that were living among plants (Dictyoptera, Orthoptera)9. The Middle Permian diversification of the small insectivorous gliding and terrestrial vertebrates probably exercised a strong selective pressure on their potential prey8, sufficient to drive the first cases of acquisition of homomorphy with plants. Disruptive coloration became also frequent among the polyneopteran insects living among plants during the Triassic9. The fact that the fossil record of disruptive coloration is clearly older than homomorphy with plants may suggest that the former strategy has lower metabolic costs and/or is much easier to evolve. The two strategies (disruptive coloration versus homomorphy) were maintained in many clades (Orthoptera, Odonata and so on) from the Mesozoic to the present. Many modern insects combine these strategies, also in association with specialized behaviors, to reduce the risk of predation32,33.