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Received 4 Jul 2016 | Accepted 28 Oct 2016 | Published 20 Dec 2016 DOI: 10.1038/ncomms13735 OPEN mimicry of plants dates back to the

Romain Garrouste1,*, Sylvain Hugel2,*, Lauriane Jacquelin1, Pierre Rostan3, J.-Se´bastien Steyer4, Laure Desutter-Grandcolas1,** & Andre´ Nel1,**

In response to predation pressure, some 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 and Permotettigonia gallica developed 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.

1 Institut de Syste´matique, E´volution, Biodiversite´, ISYEB, UMR 7205, CNRS, MNHN, UPMC, EPHE, Muse´um national d’Histoire naturelle, Sorbonne Universite´s, 57 rue Cuvier, CP 50, Entomologie, F-75005, Paris, France. 2 INCI, UPR 3212 CNRS, Universite´ de Strasbourg, 8 rue Blaise Pascal, 67084 Strasbourg, France. 3 Mines and Avenir, Les Albrands, F-05380 Chaˆteauroux Les Alpes, France. 4 Centre de Recherches en Pale´obiodiversite´ et Pale´oenvironnements, UMR 7202—CNRS, MNHN, UPMC, EPHE, Muse´um national d’Histoire naturelle, Sorbonne Universite´s, 8 rue Buffon, CP 38, F-75005 Paris, France. * These authors contributed equally to this work. ** These authors jointly supervised this work. Correspondence and requests for materials should be addressed to R.G. (email: [email protected]) or to A.N. (email: [email protected]).

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lant mimicry occurs in many clades of insects, with the a most striking cases in butterflies, praying mantises, stick Pinsects and katydids. In these groups, mimicry involves spectacular modifications of the body and wings, in response to predation. However, the accurate fossil record of plant mimicry is ScP limited to a few Cenozoic and Mesozoic taxa1–4, and is sometimes difficult to interpret5,6. In contrast, disruptive patterns of wing RP M coloration (non-homomorphous alternation of hyaline and dark transverse bands on wings) are frequent among Upper Carbo- CuA niferous flying herbivorous insects (viz. Palaeodictyoptera7), possibly because at this time the main predators of flying insects were only flying insects8. Cases of disruptive coloration b are comparatively rare among and Early Permian insects living in the vegetation (viz. Dictyoptera, )9. Gliding and terrestrial vertebrates (for example, amphibians, ScP synapsids and sauropsids) appeared or became very diverse in the RA 8,10 RP Middle Permian , in addition to the predators that RP were already present during the Carboniferous, but apparently without any particular impact on the diversification of mimicry M strategies among the insect prey. This phenomenon was supposed CuPaα 9 CuPaβ to happen during the and the . CuA+CuPaα A1 The present discovery of a Guadalupian forewing, representing CuPb the oldest katydid fossil, contradicts this view. It demonstrates c that the leaf-like homomorphous cryptic mimicry was already present 4100 million years (Ma) before the previous oldest records. This wing displays the same modifications in shape and M venation as seen in modern leaf-like katydids. It also attests that α Tettigonioidea are much older than previously thought, as this CuA+CuPa CuPaα clade was considered as not older than the Jurassic11–13. CuPaβ CuPb A1

Results Figure 1 | Permotettigonia gallica gen. et sp. nov. (a) General habitus of Systematic palaeontology. tegmen imprint. (b) Reconstruction of tegmen. (c) Detail of cubito-anal Insecta Linne´, 1758 field. Scale bar, 5 mm (a,b), 2 mm (c). Orthoptera Olivier, 1789 Chopard, 1920 Tettigonioidea Krauss, 1902 Permotettigoniidae, Nel & Garrouste fam. nov. of the katydid clade (for discussion on the other candidates Permotettigonia gallica, Nel & Garrouste gen. et sp. nov. see Supplementary Note 3). Etymology. The genus name refers to Permian and Tettigonia; the species name refers to the Latin name for Discussion France. The forewing of Permotettigonia is very broad compared Holotype. MNHN-LP-R 63853, Muse´um National d’His- with its length, only ca. 2.7 times longer than wide, with toire Naturelle, Paris, France. its surface separated into two main fields of nearly the same Horizon and locality. Red siltsones, Cians Formation, width (subcostal field and field between R and CuA of the same Roadian, Middle Permian; Doˆme de Barrot, 760 m alt., width, both 6.0 mm wide), separated by a pair of parallel Roua Valley (Supplementary Fig. 1, Supplementary Note 1), longitudinal strongly marked veins ScP and R, secondary veinlets village of Daluis, Alpes Maritimes, France. in subcostal and median fields nearly perpendicular to main Diagnosis. The fossil is a nearly complete and very broad veins, with those of subcostal field emerging obliquely from ScP tegmen (forewing) (Fig. 1) with a very broad and strongly and making a strong bend just after their base, and subcostal field corrugate field between vein subcostal posterior (ScP) and corrugated. The presence of a pronounced angle between the anal anterior wing margin, crossed by numerous long veinlets field and the rest of the tegmen suggests that the tegmina of alternatively convex and concave, all nearly perpendicular to Permotettigonia were not held horizontally but perpendicular ScP and to anterior wing margin. A second broad field is to the body. All these structures mirror those of some modern present between radial vein (R) and median vein (M) and a leaf-like macropterous Tettigoniidae14 that have an appearance of third between M and cubital complex vein (CuA þ CuPaa); upright leaves (case of occultation of the volume as relief, surface all crossed by long parallel veinlets more or less curved and and outline), for example, Pterophylla15,16, suggesting a similar perpendicular to main longitudinal veins, but not alterna- situation for Permotettigonia. tively convex and concave as in subcostal field, crossveins To examine the possibility that the tegmina of Permotettigonia present but poorly preserved in field between R and M; M could display a leaf-mimicking camouflage, we compared it with and CuA þ CuPaa simple and distally fused again; cubitus morphometric descriptors distinctive of the modern leaf- posterior (CuP) divided into branches CuPaa, CuPab and mimicking katydids. As such morphometric descriptors were CuPb, unlike in modern katydids (Supplementary Fig. 2); not already available; we performed a comprehensive morpho- anal vein A1 straight (extended description in logical analysis of the tegmina of modern katydids (data set in Supplementary Note 2). Permotettigonia is the oldest record Supplementary Table 1). Pterochrozinae is the only tettigoniid

2 NATURE COMMUNICATIONS | 7:13735 | DOI: 10.1038/ncomms13735 | www.nature.com/naturecommunications NATURE COMMUNICATIONS | DOI: 10.1038/ncomms13735 ARTICLE subfamily including only leaf-mimicking species17,18, which are 6).As the radial vein is strongly zigzagged and not thickened in considered the most perfectly camouflaged katydids. This Archepseudophylla, parameters involving this vein are not subfamily was therefore used to epitomize leaf-mimicking species. relevant to analyse this taxon. Both the circularity and the ratio We carried out morphometric analyses in a set of representa- width/length, which do not involve the radial vein, confirm that tive modern tettigoniids, including Pterochrozinae and this fossil is close to the morphology of extant mimetic species, other subfamilies with univariate (non-linear regression and but relatively less than the Permian fossil. In the morphospace of curve-fitting), bivariate (correlation between variables) and tettigoniid tegmina using PCA, it is very close to Permotettigonia multivariate (Principal Component Analysis or PCA) approaches, inside the mimetic group as defined by Mugleston et al.14 based on size-independent measures (ratios) to focus on shape (Fig. 2c). analysis. Using PCA that allows visualizing the set of all variables in the These analyses allowed to distinguish significantly two wing same space (or morphospace analysis), Permotettigonia is close to morphologies (Fig. 2; Supplementary Figs 3–8): one is corre- the centre of the set of leaf-mimicking species as defined by sponding to the tegmina of genera known for displaying leaf Mugleston et al.14 (Fig. 2c). Furthermore, if we consider a PCA mimicry (including Pterochrozinae), and the second to the non- based on the different subfamilies, Permotettigonia is between the mimetic tegmina. Distributions of morphological descriptors Pterochrozinae and the ; two clades that mainly were significantly better fitted with two components models comprise leaf-mimicking species (see Supplementary Fig. 7). having one component fixed to values obtained from Pterochro- The morphometric results strongly support the leaf mimicry zinae, than with one-component models (Supplementary function of the tegmina of Permotettigonia. The difficulty is to Table 2). For all parameters, treated with non-linear regression determine which kind of leaves Permotettigonia could have models and curve-fitting, that allow modern leaf-mimicking mimicked. Of course the angiosperms were not present species to be distinguished from other katydids, Permotettigonia during the Permian, but plants with very similar leaf or displayed values shared by at most 3% of the modern non-leaf- pseudoleaf morphology were present, symmetrical to a midvein, mimicking species and by up to 30% of modern leaf-mimicking and with subperpendicular second veins and marked species (Fig. 2a,b, Supplementary Table 3, Supplementary Figs 3– corrugations. It is especially the case of the very large angiosperm- like leaves of the Gigantopterideae and of some other tracheo- phytes lineages19–21. ab Unfortunately, no plant is recorded from the Cians Formation. Not leaf-shaped Leaf-shaped Not leaf-shaped Leaf-shaped However, two red Middle Permian palaeofloras of similar ages are known, from the Bau Rouge Member (Kungarian–Roadian22,23, 40 Permotettigonia 60 Permotettigonia Toulon Basin, Var), and the Me´rifons Member (Kungurian– 23,24 50 Capitanian , Salagou Formation, Lode`ve Basin, He´rault), at 30 All All Tettigoniidae B Pterochrozinae only 40 150 and 350 km from the Dome de Barrot. All these outcrops Pterochrozinae only 20 30 are corresponding to shallow playa lakes and submerged flood 20 25 Frequency Frequency 10 plains . 10 In the Bau Rouge Member and the Salagou Formation, the 0 0 0 0.2 0.4 0.6 0.8 1 0 0.4 0.8 1.2 1.6 Taeniopteris leaves (a type of plant ranging between the Late Width/length ratio Anterior/posterior field area ratio Paleozoic to the Mesozoic) are one of the best-known candidates c for a mimicry by Permotettigonia because they can be up to 5 cm Mimetism (Mugleston criterion) 2 wide with the surface presenting a series of corrugations tegmina shape morphometrics PCA perpendicular to a strong midvein (Supplementary Fig. 10), quite similar to the corrugations of the wing of Permotettigonia26. Also, Permotettigonia the second-order veins of the leaves of Taeniopteris are separating obliquely from the main midvein and becoming more or less nM perpendicular to the margin, quite similarly to the veinlets in the M F 1 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 insects20,28–30. 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 Figure 2 | Morphometric analyses of leaf-mimicking versus non-leaf- reconstruction in Fig. 3). It is likely that this mimicry conferred mimicking tegmina. (a,b) Non-linear regression modeling. (a) Tegmina an advantage in avoiding detection by predators, such as flying width/length ratio. (b) Anterior field area/posterior field area ratio. insects (like giant griffenflies, also recorded from the Doˆme de (c) Morphospace of tettigoniid tegmina using PCA, Ordination of 253 Barrot31) and terrestrial tetrapods. modern Tettigoniidae, the Cenozoic Archepseudophylla fossilis Nel et al., During the Late Carboniferous and the Early Permian, the 2008, plus Permotettigonia gallica, based on five morphometric indices pressure of predation on the palaeopteran flying insects by land defined in Supplementary Information. Taxa plotted in a factorial map vertebrates was probably relatively low compared with that divided into two confidence ellipses using Mugleston et al.14 criterion, nM by carnivorous flying insects, such as giant griffenflies31. The centroid of cloud of non-mimetic taxa, M centroid of cloud of mimetic taxa. plant–insect homomorphy is not recorded at that time and F Permotettigonia gallica. Values for Permotettigonia are indicated by grey disruptive coloration was relatively rare among the neopteran triangles, and white triangle for Archepseudophylla. insects that were living among plants (Dictyoptera, Orthoptera)9.

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

The Middle Permian diversification of the small insectivorous or available on OSF site32. As all parameters used for the analysis were dimension- gliding and terrestrial vertebrates probably exercised a strong free ratios calculated after our measurements, no scaling of the used images was selective pressure on their potential prey8, sufficient to drive the required. The measurements taken to calculate the ratios corresponded to general shape descriptors, with no hypothesis on homologies, except when defining the first cases of acquisition of homomorphy with plants. Disruptive anterior and the posterior fields of the tegmen, where the radius was considered coloration became also frequent among the polyneopteran insects as the limit between these fields. living among plants during the Triassic9. The fact that the fossil The measurements taken on the tegmen were: maximal length; width on the record of disruptive coloration is clearly older than homomorphy middle; anterior field width; posterior field width; total area; anterior field area; posterior field area; total perimeter; anterior field perimeter; posterior field with plants may suggest that the former strategy has lower perimeter. With these measurements, the following four dimension-free metabolic costs and/or is much easier to evolve. The two parameters were calculated: (width/length) ratio; (anterior field width/posterior strategies (disruptive coloration versus homomorphy) were field width) ratio; (anterior field area/posterior field area) ratio; and [4p(anterior 2 maintained in many clades (Orthoptera, and so on) field area)/(anterior field perimeter) ] corresponding to anterior field circularity. Tegmina were also coded as a single binary character, as being either leaf-like from the Mesozoic to the present. Many modern insects combine or not leaf-like following the criterion of Mugleston et al.14, that is, ‘leaf-like these strategies, also in association with specialized behaviors, to tegmina were defined as being oblong with the maximum width of the wing reduce the risk of predation32,33. larger than the height of the thorax, or not leaf-like, with narrow forewings that are not wider than the height of the thorax’. The values of the five parameters are listed in Supplementary Table 1. Methods The situation in our fossil is particular because the tip of its tegmen is Preparation, observation and description. The specimen was prepared using missing. Two kinds of measurements were taken: measurements with no sharp spines. Photographs were taken with a Nikon D800 digital camera with extrapolation and measurements with missing parts extrapolated with circle AF-MicroNikkor 60 mm 2.8, with dry specimens and line drawings were prepared segment connections (Supplementary Fig. 9). The parameters calculated with using a camera lucida on an Olympus SZX-9 stereomicroscope. Original photo- measurements of P. gallica were then compared with the distribution of these graphs were processed using the image-editing software Adobe Photoshop CS6. parameters in each type of tegmina (leaf-mimicking and non-leaf mimicking). The Standard wing venation nomenclature is followed for Orthoptera9. The diagnoses values for the Mugleston et al.14 criterion are unknown for P. gallica as its thorax is given in the main text are the same for the familial, generic and specific levels not preserved. because all are presently monospecific.

Morphometric analyses. Our approach is based on a data set based on 253 Nonlinear regression analyses. Analyses were performed with KyPlot 2.15 tettigoniid species that are representative of morphological disparity of macro- (KyensLab). Nonlinear regression allows defining if data distributions are signi- pterous forms. We also added the Cenozoic leaf-mimetic genus Archepseudophylla. ficantly best-described with one or with more components. We used this approach Samples of all modern tettigoniid subfamilies were included to assess whether morphologically distinct types of forewings can be distinguished in the analysis, except exclusively micropterous or apterous subfamilies. The and whether one of the forewing types includes all Pterochrozinae, a subfamily established morphospace expresses a gradient from forms considered non-mimetic epitomizing leaf-mimicking species. towards forms that are extremely mimetic of leaves of angiosperms (morphological The cumulative distribution of each dimension-free parameter calculated patterns, colours and associated behaviour). Measurements were performed with measurements described above was fitted using nonlinear regression34. with ImageJ 1.46r (NIH) software, on drawings or pictures of tegmina, either Cumulative distribution was used to avoid the loss of information induced by from collection specimens (S.H. collection, or Muse´e Zoologique de Strasbourg) data binning.

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The cumulative distribution of each parameter of all measured Tettigoniidae 2. Jarzembowski, E. A. Fossil cockroaches or pinnule insects? Proc. Geol. Assoc. was first fitted with the following single-cumulative distribution function of the 105, 305–311 (1994). normal distribution. 3. Wang, Y.-J. et al. Ancient pinnate leaf mimesis among lacewings. Proc. Natl One component model:  Acad. Sci. USA 107, 16212–16215 (2010). 1 x A1 4. Shcherbakov, D. E. New and little-known families of Hemiptera Cicadomorpha FxðÞ¼; A1; A2 1 þ erf p ð1Þ 2 A2 2 from the Triassic of Central Asia—early analogs of treehoppers and planthoppers. Zootaxa 2836, 1–26 (2011). where A1 is the mean; A2 is the standard deviation; erf is Gauss error function. 5. Prokop, J. et al. New middle Permian insects from Salagou Formation of the To define characteristics of epitomized leaf-mimicking forewings, we fitted Lode`ve Basin in southern France (Insecta: Pterygota). Ann. Soc. Entomol. the cumulative distribution of each parameter from Pterochrozinae with the France 51, 14–51 (2015). same cumulative distribution function of the normal distribution (equation (1)). We 6. Wang, Y.-J. et al. Jurassic mimicry between a hangingfly and a ginkgo from considered the parameters obtained with that fitting as characteristic of leaf-mimicking China. Proc. Natl Acad. Sci. USA 109, 20514–20519 (2012). tegmina. 7. Li, Y.-J. et al. A new palaeodictyopterid (Insecta: Palaeodictyoptera: The mean (A1) obtained from that single-component fitting of Pterochrozinae parameters was then forced as the mean one of the two components of the Spilapteridae) from the Upper Carboniferous of China supports a close following function used to fit each parameter of all measured Tettigoniidae. relationship between insect faunas of Quilianshian (northern China) and Two components model, one component forced to Pterochrozinae mean: Laurussia. Alcheringa 37, 487–495 (2013).   8. Steyer, J.-S. Earth Before the Dinosaurs (Indiana Univ. Press, 2012). 1 x A3 FxðÞ¼; A1; A2; A3; A4; A5 A5 1 þ erf p 9. Gorochov, A. V. & Rasnitsyn, A. P. in History of Insects (eds Rasnitsyn, A. P. 2 A4 2 & Quicke, D. L. J.). 293–304 (Kluwer Academic Publishers, 2002). ð2Þ x A1 10. Modesto, S. P. et al. Arthropod remains in the oral cavities of fossil reptiles þ ðÞ1 A5 1 þ erf p A2 2 support inference of early insectivory. Biol. Lett. 5, 838–840 (2009). 11. Gorochov, A. V. in Melovoj Biotsenoticheskij Krizis i Evolutsiya Nasekomykh. where A1 is the mean obtained by fitting Pterochrozinae parameters with biocoenotic crisis and insect evolution. (ed. Ponomarenko, A. G.) equation (1); A2 is the standard deviation of the component with forced A1; 1–230 (Nauka, 1988). A3 and A4 are, respectively, the mean and the s.d. of the other component; 12. Gorochov, A. V. Sistema i evolyutsiya pryamokrylykh podotryada Ensifera (1 A5) is the relative contribution of the component forced to Pterochrozinae (Orthoptera) System and Evolution of the suborder Ensifera (Orthoptera). mean; A5 is the contribution of the other component. Parts 1 and 2. Trudy Zool. Inst. 260, 3–224 261: 3–212 (1995). We then compared which of the single component model or the two 13. Gorochov, A. V. Review of Triassic Orthoptera with descriptions of new and components model (equation (1) versus equation (2)) was best describing the little known taxa: part 2. Paleontol. J. 39, 272–279 (2005). distributions of all measured Tettigoniidae using the extra sum-of-squares F test 14. Mugleston, J. D. et al. A century of paraphyly: A molecular phylogeny of with a threshold of significance set at P 0.01, as well as decreases in Akaike’s o katydids (Orthoptera: Tettigoniidae) supports multiple origins of leaf-like Information Criterion and Bayesian Information Criterion. Should the two wings. Mol. Phylogenet. Evol. 69, 1120–1134 (2013). components model be significantly better than the single-component model, it 15. Beier, M. Orthoptera Tettigoniidae (Pseudophyllinae I and II). Das Tierreich would allow defining the mean and the s.d. of each parameter for the two types of tegmina: leaf-mimicking and non-leaf-mimicking. 73–74, 1–468 1–396 (1962). Although cumulative distribution of the parameters was used for the analysis, 16. Leroy, Y. Le camouflage chez les sauterelles Tettigonioidea. Bull. Soc. Entomol. binned data were represented in the figures together with a Gaussian distribution France 90, 1051–1071 (1985). having the parameters obtained with the fitting of the cumulative distribution. 17. Vignon, P. Le camouflage . Nature 59, 1–5 (1931). 18. Braun, H. Little walking leaves from southeast Ecuador: biology and of Typophyllum species (Orthoptera, Tettigoniidae, Pterochrozinae). Zootaxa Morphospace representation using multivariate statistic ordination. A morp- 4012, 21–32 (2015). hospace is a practical or theoretical mathematical space for study the phenotypes 19. Glasspool, I. J. et al. Foliar physiognomy in Cathaysian gigantopterids and the of living or fossil organisms, widely used in zoology, botany and evolutionary 35–37 potential to track Palaeozoic climates using an extinct plant group. Palaeogeogr. biology . In theoretical morphospaces, the axes of the reduced space are Palaeoclimatol. Palaeoecol. 205, 69–110 (2004). determined by a small set of parameters of morphogenetic or other biological 20. Glasspool, I. et al. Foliar herbivory in the Late Palaeozoic Cathaysian models, derived from theoretical considerations rather than from the organisms gigantopterids. Rev. Palaeobot. Palynol. 127, 125–132 (2003). themselves. In morphometric (or empiric) morphospaces, it is often not trivial 21. Xue, J.-H. et al. Stepwise evolution of Paleozoic tracheophytes from South China: to choice a particular type of variables and metrics that properly reflect the studied contrasting leaf disparity and taxic diversity. Earth Sci. Rev. 148, 77–93 (2015). developmental, functional, or evolutionary properties and traits of the organisms. ´ ´ This choice is a compromise between accessible characters and scope. For 22. Durand, M. Un exemple de sedimentation continentale permienne dominee fossil studies, this is particularly delicate as it is dependent of the quality of par l’activite´ de chenaux me´andriformes: la formation de Saint-Mandrier preservation. The structure of a morphospace is also determined by the choice (bassin de Toulon, Var). Ge´ol. France 1993, 43–55 (1993). of the characters to include, by the way these characters are coded, and by the 23. Evans, M. E. et al. Late Permian paleomagnetic results from the Lode`ve, method of visualization/construction of the space36. The PCA ordination method38 Le Luc, and Bas-Argens Basins (southern France): magnetostratigraphy and is a widely used multivariate statistics method which creates a low-dimension geomagnetic field morphology. Phys. Earth Planet. Inter. 237, 18–24 (2014). ordination that maximizes the variation between measured specimens17,19, and 24. Pochat, S. & Van Den Driessche, J. Filling sequence in Late Paleozoic creates a visualization by a projection (two or three axes, or 3D outputs). The continental basins: A chimera of climate change? A new light shed given by the PCA was performed using R software, package ADE4 (refs 39–41) and RStudio42. Graissessac–Lode`ve basin (SE France). Palaeogeogr. Palaeoclimatol. Palaeoecol. Graphic displays have been modified in Adobe Illustrator CS6. 302, 170–186 (2011). The PCA was performed using R software, package ADE4 (ref. 41). 25. Haldan, M. M. et al. comparison of detailed equatorial red bed records of secular variation during the Permo-Carboniferous Reversed Superchron. Geophys. J. Int. 177, 834–848 (2009). Nomenclatural acts. This published work and the nomenclatural acts it contains 26. Galtier, J. & Broutin, J. Floras from red beds of the Permian Basin of Lode`ve have been registered in ZooBank, the proposed online registration system for the International Code of Zoological Nomenclature (ICZN). The ZooBank LSIDs (Life (Southern France). J. Iber. Geol. 34, 57–72 (2008). Science Identifiers) can be resolved and the associated information viewed through 27. Rentz, D. C. F., Su, Y.-N. & Ueshima, N. Studies in Australian Tettigoniidae: any standard web browser by appending the LSID to the prefix http://zoobank.org/. The mecopodine katydids. Part 2 (Orthoptera: Tettigoniidae; ; The ZooBank LSIDs (Life Science Identifiers) for the new family, genus and Sexavaini) Queensland palm katydid. Trans. Am. Entomol. Soc. 132, 229–241 species are as follows: urn:lsid:zoobank.org:act:831FB4B9-A27A-4A43-989E- (2006). D74F26B42C19, urn:lsid:zoobank.org:act:654E7DAC-083B-4F43-B32B- 28. Schachat, S. R. et al. Plant-insect interactions from Early Permian 8E4DE28F3877 and urn:lsid:zoobank.org:act:5B6A3647-A015-46D2-BC60- (Kungurian) Colwell Creek Pond, North-Central Texas: the early spread E0B826C2BDE2. of herbivory in riparian environments. Int. J. Plant Sci. 175, 855–890 (2014). 29. Beck, A. L. & Labandeira, C. C. Early Permian insect folivory on a gigantopterid-dominated riparian flora from north-central Texas. Palaeogeogr. Data availability All relevant data are available from the authors. The specimen . Palaeoclimatol. Palaeoecol. 142, 139–173 (1998). MNHN-LP-R 63853 is housed at the Muse´um National d’Histoire Naturelle 30. Jarzembowski, E. A. The oldest plant-insect interaction in Croatia: (MNHN), Paris, France. Carboniferous evidence. Geol. Croat. 65, 387–392 (2012). 31. Nel, A. et al. Revision of Permo-Carboniferous griffenflies (Insecta: References Odonatoptera: Meganisoptera) based upon new species and redescription of 1. Wedmann, S. A brief review of the fossil history of plant masquerade by insects. selected poorly known taxa from Eurasia. Palaeontographica (A) 289, 89–121 Palaeontographica (B) 283, 175–182 (2010). (2009).

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32. Stevens, M. & Cuthill, I. C. Disruptive coloration, crypsis and edge detection also thank the ‘Muse´eZoologiquedelaVilleetdel’Universite´ de Strasbourg’ for giving in early visual processing. Proc. R. Soc. (B) 273, 2141–2147 (2006). access to their collections and J.L. Rodeau for discussions on non-linear regression modelling. 33. Eades, D. C. et al.Orthoptera Species File. Version 5.0/5.0 http://Orthoptera.SpeciesFile.org (2016). Author contributions 34. Motulsky, H. & Christopoulos, A. Fitting models to biological data using R.G. and S.H. performed the morphometric analyses; A.N., L.D.-G., S.H., R.G., P.R., linear and nonlinear regression. A Practical Guide to Curve Fitting (GraphPad J.-S.S., L.J. prepared the manuscript; S.H., L.J. and R.G. prepared the figures, P.R. dis- Software Inc. www.graphpad.com, 2003). covered the fossil; A.N. and R.G. designed the program; L.D.-G. and A.N. jointly 35. Mitteroecker, P. & Huttegger, S. M. The concept of morphospaces in supervised this work. evolutionary and developmental biology: mathematics and metaphors. Biol. Theory 4, 54–67 (2009). 36. Mitteroecker, P. & Bookstein, F. L. Linear discrimination, ordination, and the Additional information 38, visualization of selection gradients in modern morphometrics. Evol. Biol. Supplementary Information accompanies this paper at http://www.nature.com/ 100–114 (2011). naturecommunications 37. Chartier, M. et al. The floral morphospace—a modern comparative approach to study angiosperm evolution. New Phytol. 204, 841–853 (2014). Competing financial interests: The authors declare no competing financial 38. Jolliffe, I. T. Principal Component Analysis (Springer Series in Statistics, interests. 2002). 39. R Development Core Team. R: A language and environment for statistical Reprints and permission information is available online at http://npg.nature.com/ computing (R Foundation for Statistical ComputingISBN 3-900051-07-0URL reprintsandpermissions/ http://www.R-project.org, 2008). How to cite this article: Garrouste, R. et al. Insect mimicry of plants dates back to the 40. Chessel, D. et al. The ADE4 package-I- One-table methods. RNews4, 5–10 (2004). Permian. Nat. Commun. 7, 13735 doi: 10.1038/ncomms13735 (2016). 41. Dray, S. & Dufour, A. B. The ADE4 package: implementing the duality diagram for ecologists. J. Stat. Softw. 22, 1–20 (2007). Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in 42. RStudio Team. RStudio: Integrated Development for R (RStudio, Inc. Available published maps and institutional affiliations. at http://www.rstudio.com/, 2015).

This work is licensed under a Creative Commons Attribution 4.0 Acknowledgements International License. The images or other third party material in this This work was supported by a grant from Agence Nationale de la Recherche under the article are included in the article’s Creative Commons license, unless indicated otherwise LabEx ANR-10-LABX-0003-BCDiv, in the program ‘Investissements d’avenir’ ANR-11- in the credit line; if the material is not included under the Creative Commons license, IDEX-0004-02 (Labex BCDiv ‘Diversite´ Biologique et Culturelle’) and by the ATM ‘Blanc’ users will need to obtain permission from the license holder to reproduce the material. MNHN 2015-2016. Many thanks to C. Garrouste for the reconstruction of To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ Permotettigonia gallica and to S. Fouche´ (Muse´edeLode`ve) for the photograph of the plant Taeniopteris sp. from Lode`ve. Many thanks to B. Warren (University of Zurich) for judicious and important comments on the preliminary version of the paper. We r The Author(s) 2016

6 NATURE COMMUNICATIONS | 7:13735 | DOI: 10.1038/ncomms13735 | www.nature.com/naturecommunications 1

Supplementary Figures

Supplementary Figure 1 | The Roua valley outcrop (alt. 760 m). Cians Formation, Dôme de Barrot. Place of discovery of Permottetigonia gallica (arrow). Thickness of visible deposit ca. 500 m (alt. 700 m to 1200 m).

1 2

Supplementary Figure 2 | imperialis (White, 1846). Tegmen base. M median vein,

CuA convex cubitus anterior, CuP concave cubitus posterior, A1 convex first anal vein. Scale bar, 2 mm.

2 3

Supplementary Figure 3 | Morphometric descriptor: anterior field circularity.

Pterochrozinae used to epitomize modern leaf-mimicking katydids. (a) Cumulative distribution of morphometric descriptors from Pterochrozinae (in grey) fitted with a single component function (in red) (equation 1). (b)

Cumulative distribution of corresponding morphometric descriptors of all analyzed taxa fitted with a two component function (in red), with mean of one component forced to that obtained from Pterochrozinae. (c) Two cumulative distributions of morphometric descriptors from Pterochrozinae (in green) and all analyzed

Tettigoniidae (in grey) represented at same scale together with values from Permotettigonia gallica (yellow bars). (d) Histogram constructed with cumulative distributions illustrated in (a-c); black curve corresponds to two components fitting of cumulative distribution illustrated in (b) and converted to frequency distribution. (e)

Distribution of parameters from non-leaf-mimicking species, extracted from first component of curve in (d). (f)

Distribution of parameters from leaf-mimicking species, extracted from second component of curve in (d). This component has a mean forced to values obtained from Pterochrozinae alone (red curve in a). Values for P. gallica are indicated by yellow bars, and values for A. fossilis are indicated by grey triangles.

3 4

Supplementary Figure 4 | Morphometric descriptor: (anterior field area /posterior field area) ratio. Same legend as for Supplementary Figure 3.

4 5

Supplementary Figure 5 | Morphometric descriptor: (posterior field width /anterior field width) Ratio. Same legend as for Supplementary Figure 3.

5 6

Supplementary Figure 6 | Morphometric descriptor: ratio (width/length). Same legend as for Supplementary Figure 3.

6 7

Supplementary Figure 7 | Systematics tegmina shape morphometrics (PCA). a. Factorial map on the plan 1-2 (x= axis 1, y= axis 2) organized by subfamilies. Confidence ellipses: 67% of the taxa in each subfamily. Labels of subfamilies located at their centroids. acri

Acridoxeninae, cono , hex Hexacentrinae, list Listroscelidinae, meco

Mecopodinae, phan , phyllo , pseu Pseudophyllinae, ptero

Pterophyllinae, tymp Tympanophorinae, tetti Tettigoniinae, zapro Zaprochilinae. F Fossil. b.

Correlation circle of morphometric indices in plan 1-2 of the PCA. CircCA anterior field circularity, CircCP posterior field circularity, RapL.l (width/length) ratio, RaplargAP (anterior field width/posterior field width) ratio, RapAire.CACP (posterior field surface/anterior field surface) ratio. c. Eigenvalues of PCA, showing clear domination of axis 1 and axis 2 (86% of total inertia).

7 8

Supplementary Figure 8 | Correlations between variables. Bivariate relationships between the morphometric variables using Pearson correlation test, statistical significance indicated by the grey levels. R correlation value, * significant (0.01

(<0.001). CircCA anterior field circularity, CircCP posterior field circularity, RapL.l

(width/length) ratio, RaplargAP (anterior field width/posterior field width) ratio,

RapAire.CACP (posterior field surface /anterior field surface) ratio.

8 9

Supplementary Figure 9 | Extrapolations of missing parts of Permotettigonia gallica. (a)

Measurements taken directly on the fossil, with no extrapolation and linear joining of missing parts. (b) Measurements taken with missing parts extrapolated with circle segment connections. Anterior field area in grey.

9 10

Supplementary Figure 10 | Taeniopteris sp. from Lodève. Leaf with intact apical region and narrow midvein, subperpendicular second order veins, and marked corrugations; specimen MULOD 1236 (Lodève Museum, France). Scale bar, 2 mm.

10 11

Sample name Mugl. Subfamily GEOMETRY PF/AF W/L AFA/PFA Velella cruenta 0 Phaneropterinae 0,103 4,431 0,232 0,225 Phaneroptera nana 0 Phaneropterinae 0,130 3,804 0,192 0,246 Cratioma aberratum 1 Pseudophyllinae 0,144 0,167 0,346 0,286 Cnemidophyllum sp 1 Phaneropterinae 0,175 2,518 0,346 0,316 Phaneroptera falcata 0 Phaneropterinae 0,147 3,851 0,203 0,324 Leptotettix voluptarius 1 Pseudophyllinae 0,125 0,324 0,204 0,336 Leptotettix pubiventris 1 Pseudophyllinae 0,144 0,414 0,212 0,354 Conocephalus fuscus 0 Conocephalinae 0,111 1,896 0,143 0,364 Platychiton brunneus 1 Pseudophyllinae 0,139 0,468 0,202 0,371 Tylopsis lilifolia 0 Phaneropterinae 0,097 2,096 0,143 0,372 Xiphidiopsis lita 0 Meconematinae 0,086 3,628 0,112 0,374 Brachyphisis nattecantor 0 Meconematinae 0,158 2,308 0,237 0,395 Steirodon dentiferum 1 Phaneropterinae 0,225 2,015 0,285 0,402 Platycleis sabulosa 0 Tettigoniinae 0,112 2,084 0,126 0,407 Seselphisis visenda 0 Meconematinae 0,109 2,136 0,131 0,413 Stilpnochlora marginella 1 Phaneropterinae 0,231 0,462 0,376 0,416 Chondrosternum triste 1 Pseudophyllinae 0,175 0,539 0,235 0,418 Ruspolia nitidula 0 Conocephalinae 0,099 1,960 0,119 0,427 viridivitta 1 Pseudophyllinae 0,170 0,897 0,237 0,431 Conocephalus iris 0 Conocephalinae 0,111 1,997 0,131 0,431 Mioacris longicauda 1 Pseudophyllinae 0,202 0,525 0,246 0,439 Platycleis albopunctata 0 Tettigoniinae 0,119 1,636 0,155 0,439 Phylloptera sp. 1 Phaneropterinae 0,190 2,286 0,278 0,445 Conocephalus cinereus 0 Conocephalinae 0,140 1,430 0,142 0,447 Peucestes cristatissimus 1 Phaneropterinae 0,215 0,461 0,373 0,448 Neoconocephalus triops 0 Conocephalinae 0,113 2,153 0,143 0,456 Mustius afzelii 1 Pseudophyllinae 0,233 0,469 0,374 0,460 Platycleis tessellata 0 Tettigoniinae 0,119 1,647 0,138 0,461 Macrochiton heros 1 Pseudophyllinae 0,176 0,424 0,232 0,464 Morsimus areatus 1 Pseudophyllinae 0,221 0,464 0,304 0,488 Pseudophyllus colosseus 1 Pseudophyllinae 0,199 0,525 0,359 0,503 Decticus verrucivorus 0 Tettigoniinae 0,177 1,829 0,216 0,504 Redtenbachus viridipennis 0 Conocephalinae 0,118 1,834 0,144 0,504 Tettigonia viridissima 0 Tettigoniinae 0,159 1,721 0,190 0,505 Decticus albifrons 0 Tettigoniinae 0,142 1,532 0,174 0,505 Pseudophyllus colosseus Male 1 Pseudophyllinae 0,197 0,484 0,368 0,511 Acauloplacella immunis 1 Pseudophyllinae 0,224 0,602 0,324 0,533 Xerophyllopteryx fumosa 1 Pseudophyllinae 0,196 0,575 0,272 0,540 Cnemidophyllum citrifolium 1 Phaneropterinae 0,264 0,853 0,341 0,542 Pterochroza ocellata 1 Pterochrozinae 0,307 0,511 0,433 0,543 Olcinia pallidifrons 1 Pseudophyllinae 0,201 0,477 0,262 0,544 Phyllopectis crepitans 1 Pseudophyllinae 0,428 0,892 0,589 0,554 Nannonotus alatus 0 Pseudophyllinae 0,170 0,835 0,214 0,567 Mioacris javanum Femelle 1 Pseudophyllinae 0,233 0,599 0,324 0,569 Neoconocephalus affinis 0 Conocephalinae 0,127 1,361 0,120 0,578 Acauloplacella insularis 1 Pseudophyllinae 0,237 0,503 0,329 0,580 Tympanoptera angustipennis 1 Pseudophyllinae 0,195 0,648 0,253 0,591 Pterophylla baez 1 Pseudophyllinae 0,373 1,004 0,504 0,600 Tympanophyllum imperfectum 1 Pseudophyllinae 0,265 0,543 0,411 0,602 12

Lonchitophyllum reticulatum 1 Pseudophyllinae 0,351 0,661 0,453 0,613 Phyllomimus ampullatus 1 Pseudophyllinae 0,238 0,617 0,289 0,624 Tettigonia cantans 1 Tettigoniinae 0,319 1,164 0,392 0,632 Pterophylla beltrani 1 Pseudophyllinae 0,347 1,229 0,344 0,643 Mioacris javana 1 Pseudophyllinae 0,294 0,714 0,374 0,673 Tanusia brullaei 1 Pterochrozinae 0,451 0,832 0,594 0,696 Promeca pulchellerima 1 Pseudophyllinae 0,279 0,779 0,331 0,702 Sikoriella bimaculata 1 Phaneropterinae 0,310 1,095 0,349 0,705 Roxelana crassicornis 1 Pterochrozinae 0,526 0,864 0,824 0,738 Wattenwylella dispar 1 Pseudophyllinae 0,405 0,813 0,568 0,810 Mimetica imperatrix 1 Pterochrozinae 0,467 0,870 0,594 0,819 Anommatoptera ingens 1 Pterochrozinae 0,425 1,119 0,541 0,866 Parasimodera saussurei 1 Pseudophyllinae 0,384 1,179 0,419 0,943 Mimetica pehlkei 1 Pterochrozinae 0,386 0,984 0,490 0,956 Ommatoptera pictifolia 1 Pterochrozinae 0,410 0,993 0,447 0,960 Paracycloptera grandifolia 1 Pterochrozinae 0,407 0,946 0,526 0,999 Typophyllum erosum 1 Pterochrozinae 0,404 0,950 0,579 1,027 Narea elongata 1 Pseudophyllinae 0,320 1,018 0,379 1,051 Porphyromma speciosa 1 Pterochrozinae 0,520 0,971 0,593 1,147 Mimetica viridifolia 1 Pterochrozinae 0,563 1,442 0,637 1,232 Simodera acutifolia 1 Pseudophyllinae 0,314 1,167 0,427 1,260 Mastophyllum scabricolle 1 Pseudophyllinae 0,355 0,732 0,290 1,341 Cycloptera speculata 1 Pterochrozinae 0,490 0,718 0,578 1,465 Typophyllum trigonium 1 Pterochrozinae 0,387 1,142 0,552 1,476 Aganacris sp. 0 Phaneropterinae 0,120 0,367 0,215 0,325 Sylvainhugiella cesairei 0 Conocephalinae 0,129 0,641 0,127 0,608 Amblycorypha oblongifolia 1 Phaneropterinae 0,198 0,469 0,324 0,377 Anaulocomera sp. 0 Phaneropterinae 0,137 0,360 0,190 0,369 Brachyphisis viettei 0 Meconematinae 0,158 0,319 0,228 0,326 Caulopsis sp. 0 Conocephalinae 0,049 0,142 0,072 0,274 Cnemidophyllum lineatum 1 Phaneropterinae 0,169 0,402 0,279 0,354 Conocephalus fasciatus 0 Conocephalinae 0,104 0,578 0,124 0,446 Cophipora cornuta 1 Conocephalinae 0,198 0,757 0,189 0,744 Cophipora longicauda 1 Conocephalinae 0,174 0,634 0,176 0,670 Eurycorypha prasinata 1 Phaneropterinae 0,195 0,547 0,287 0,419 Holochlora biloba 1 Phaneropterinae 0,161 0,460 0,261 0,403 Meconema thalassinum 0 Meconematinae 0,203 0,683 0,260 0,508 Moncheca sp. 0 Conocephalinae 0,132 0,387 0,177 0,499 Neoconocephalus ensiger 0 Conocephalinae 0,132 0,502 0,157 0,490 Oxyprora sp. 0 Conocephalinae 0,151 0,479 0,202 0,420 Phisis holdhausi 0 Meconematinae 0,089 0,265 0,103 0,409 Pseudorhynchus lessonnii 0 Conocephalinae 0,079 0,251 0,112 0,327 Pycnopalpa sp. 1 Phaneropterinae 0,136 0,415 0,251 0,320 Ruspolia differens 0 Conocephalinae 0,099 0,489 0,116 0,442 Seselphisis sp. 0 Meconematinae 0,087 0,374 0,117 0,374 Viadana sp. 1 Phaneropterinae 0,261 0,772 0,374 0,571 Anommatoptera hoegei 1 Pterochrozinae 0,397 1,169 0,557 0,807 Anommatoptera ingens 1 Pterochrozinae 0,422 1,002 0,553 0,842 Anommatoptera maculifolia 1 Pterochrozinae 0,406 1,135 0,548 0,761 Anommatoptera ochracea 1 Pterochrozinae 0,349 1,075 0,496 0,720 13

Celidophylla albimacula 1 Pterochrozinae 0,329 1,408 0,407 0,649 Cycloptera arcuata 1 Pterochrozinae 0,441 0,819 0,587 1,293 Mimetica angulosa 1 Pterochrozinae 0,430 0,877 0,567 0,950 Mimetica aridifolia 1 Pterochrozinae 0,419 0,792 0,474 1,274 Mimetica casanea 1 Pterochrozinae 0,463 0,847 0,567 1,149 Mimetica imperatrix 1 Pterochrozinae 0,524 0,833 0,601 1,234 Mimetica incisa 1 Pterochrozinae 0,483 0,756 0,582 1,151 Mimetica stigmatica 1 Pterochrozinae 0,447 0,739 0,551 1,392 Mimetica subintegra 1 Pterochrozinae 0,512 0,694 0,621 1,366 Mimetica tuberata 1 Pterochrozinae 0,402 0,772 0,637 0,948 Ommatoptera elegans 1 Pterochrozinae 0,375 0,931 0,445 0,979 Ommatoptera laurifolia 1 Pterochrozinae 0,391 0,885 0,383 1,039 Ommatoptera mutila 1 Pterochrozinae 0,499 1,094 0,542 0,836 Porphyromma viridifolia 1 Pterochrozinae 0,458 1,033 0,593 0,884 Rhodopteryx hebardi 1 Pterochrozinae 0,393 1,323 0,608 0,620 Tanusia arrosa 1 Pterochrozinae 0,345 1,387 0,511 0,596 Tanusia colorata 1 Pterochrozinae 0,386 1,547 0,566 0,627 Tanusia corrupta 1 Pterochrozinae 0,343 1,443 0,528 0,632 Tanusia cristata 1 Pterochrozinae 0,331 1,301 0,527 0,575 Tanusia decorata 1 Pterochrozinae 0,357 1,281 0,504 0,645 Tanusia illusyrata 1 Pterochrozinae 0,384 1,405 0,537 0,655 Tanusia signata 1 Pterochrozinae 0,365 1,171 0,551 0,600 Tanusia undulata 1 Pterochrozinae 0,369 1,115 0,564 0,720 Tanusia versicolor 1 Pterochrozinae 0,372 1,238 0,534 0,699 Typophyllum bolivari 1 Pterochrozinae 0,287 1,490 0,563 0,573 Typophyllum champenoisi 1 Pterochrozinae 0,392 1,336 0,541 0,687 Typophyllum chlorophyllum 1 Pterochrozinae 0,379 1,927 0,647 0,485 Typophyllum cinnamum 1 Pterochrozinae 0,361 1,287 0,611 0,718 Typophyllum columbicum 1 Pterochrozinae 0,463 0,969 0,555 1,086 Typophyllum eeckei 1 Pterochrozinae 0,422 0,956 0,537 1,053 Typophyllum egregium 1 Pterochrozinae 0,401 1,125 0,578 0,762 Typophyllum erosifolium 1 Pterochrozinae 0,476 0,820 0,493 1,083 Typophyllum flavifolium 1 Pterochrozinae 0,476 1,077 0,585 1,059 Typophyllum geminum 1 Pterochrozinae 0,372 1,331 0,698 0,646 Typophyllum helleri 1 Pterochrozinae 0,398 0,925 0,567 1,098 Typophyllum histrio 1 Pterochrozinae 0,424 1,070 0,584 0,862 Typophyllum inflatum 1 Pterochrozinae 0,457 1,308 0,570 1,121 Typophyllum laciniosum 1 Pterochrozinae 0,471 0,903 0,474 1,492 Typophyllum lacinipenne 1 Pterochrozinae 0,425 1,158 0,493 0,926 Typophyllum morrisi 1 Pterochrozinae 0,421 0,692 0,682 0,960 Typophyllum mortuifolium 1 Pterochrozinae 0,485 1,185 0,684 0,850 Typophyllum mutilatum 1 Pterochrozinae 0,383 0,995 0,496 0,875 Typophyllum onkiosternum 1 Pterochrozinae 0,254 1,346 0,502 0,477 Typophyllum praeruptum 1 Pterochrozinae 0,359 1,196 0,439 1,244 Typophyllum scissifolium 1 Pterochrozinae 0,442 0,955 0,536 1,160 Typophyllum trapeziforme 1 Pterochrozinae 0,396 1,099 0,580 0,900 Typophyllum trigonum 1 Pterochrozinae 0,389 0,800 0,627 1,342 Typophyllum vignoni 1 Pterochrozinae 0,290 1,117 0,538 0,667 Abaxisotima furca 1 Phaneropterinae 0,073 0,103 0,234 0,163 Aegimia cultrifera 1 Phaneropterinae 0,280 0,473 0,487 0,445 14

Aegimia elongata 1 Phaneropterinae 0,242 0,434 0,424 0,400 Aegimia maculifolia 1 Phaneropterinae 0,283 1,994 0,430 0,441 Aegimia venarecta 1 Phaneropterinae 0,276 0,528 0,453 0,448 Aganacris nitida 0 Phaneropterinae 0,124 0,418 0,227 0,265 Aganacris velutina 0 Phaneropterinae 0,112 0,277 0,203 0,225 Agaurella mirabilis 1 Phaneropterinae 0,287 0,292 0,563 0,306 Anapolisia micromargaritifera 1 Phaneropterinae 0,238 0,581 0,314 0,296 Anapolisia senta 1 Phaneropterinae 0,256 0,558 0,372 0,321 Anapolisia zonata 1 Phaneropterinae 0,199 0,449 0,368 0,244 Anaulacomera libidinosa 1 Phaneropterinae 0,204 0,686 0,253 0,524 Anaulacomera pallens 1 Phaneropterinae 0,152 0,381 0,209 0,362 Ancylecha fenestrata 1 Phaneropterinae 0,260 0,487 0,466 0,434 Apoballa errabunda 1 Phaneropterinae 0,156 0,340 0,287 0,255 Apocerycta bariana 1 Phaneropterinae 0,218 0,549 0,321 0,423 Arantia hydatinoptera 1 Phaneropterinae 0,160 0,416 0,200 0,405 Arantia accrana 1 Phaneropterinae 0,199 0,578 0,248 0,391 Arantia excelsior 1 Phaneropterinae 0,184 0,604 0,264 0,473 Arantia fasciata 1 Phaneropterinae 0,248 0,688 0,321 0,496 Arantia leptocnemis 0 Phaneropterinae 0,112 0,296 0,157 0,325 Arantia orthocnemis 0 Phaneropterinae 0,140 0,502 0,209 0,387 Arantia simplicinervis 1 Phaneropterinae 0,108 0,336 0,160 0,293 Arantia fatidica 1 Phaneropterinae 0,166 0,406 0,210 0,430 Arnobia trichopus 1 Phaneropterinae 0,135 0,352 0,199 0,312 Baryprostha bellua 1 Phaneropterinae 0,272 0,470 0,446 0,347 Caedicia albidiceps 0 Phaneropterinae 0,115 0,223 0,195 0,177 Caedicia congrua 0 Phaneropterinae 0,175 0,395 0,229 0,335 Caedicia pictipes 0 Phaneropterinae 0,142 0,355 0,160 0,408 Casigneta bisinuata 0 Phaneropterinae 0,106 0,294 0,157 0,357 Casigneta cochleata 0 Phaneropterinae 0,131 0,269 0,196 0,281 Catoptropteryx capreola 0 Phaneropterinae 0,106 0,349 0,182 0,291 Catoptropteryx guttatipes 0 Phaneropterinae 0,107 0,289 0,166 0,300 Ceraia beckeri 1 Phaneropterinae 0,111 0,340 0,236 0,243 Cesasundana producta 0 Phaneropterinae 0,088 0,216 0,127 0,286 Dapanera genuteres 1 Phaneropterinae 0,175 0,481 0,276 0,373 Diogena fausta 0 Phaneropterinae 0,137 0,248 0,164 0,319 Ducetia japonica 0 Phaneropterinae 0,117 0,383 0,182 0,410 Dysmorpha obesa 1 Phaneropterinae 0,379 0,546 0,472 0,412 Dysonia diffusa 1 Phaneropterinae 0,085 0,224 0,183 0,201 Elbenia nigrosignata 0 Phaneropterinae 0,101 0,201 0,156 0,230 Elimaea (Elimaea) thaii 0 Phaneropterinae 0,076 0,315 0,121 0,323 Elimaea obtusilota 0 Phaneropterinae 0,127 0,422 0,192 0,337 Enochletica ostentatrix 1 Phaneropterinae 0,144 0,424 0,272 0,301 Euceraia atrosignata 0 Phaneropterinae 0,090 0,331 0,189 0,222 Eulioptera monticola 0 Phaneropterinae 0,114 0,362 0,168 0,295 Euthyrrhachis gracilis 0 Phaneropterinae 0,084 0,286 0,133 0,316 Holochlora paradoxa 1 Phaneropterinae 0,128 0,303 0,210 0,300 Holochlora venosa 1 Phaneropterinae 0,141 0,397 0,206 0,363 Phylloptera difficilis 1 Phaneropterinae 0,208 0,350 0,331 0,292 Hyperphrona nitidipennis 0 Phaneropterinae 0,127 0,162 0,306 0,224 Amacroxiphus nigrifrons 0 Conocephalinae 0,120 0,379 0,130 0,470 15

Axylus bimaculatus 0 Conocephalinae 0,151 0,669 0,143 0,630 Axylus castaneus 0 Conocephalinae 0,144 0,423 0,175 0,405 Axylus thoracicus 0 Conocephalinae 0,147 0,430 0,161 0,476 Clasma parcispinosa 0 Conocephalinae 0,131 0,437 0,151 0,426 Coniungoptera nothofagi 0 Conocephalinae 0,235 0,627 0,275 0,537 Eppia truncatipennis 0 Conocephalinae 0,153 0,428 0,166 0,520 Eppioides malaya 0 Conocephalinae 0,126 0,422 0,167 0,401 Eulobaspis moluccana 0 Conocephalinae 0,179 0,631 0,173 0,544 Eulobaspis personata 0 Conocephalinae 0,193 0,716 0,159 0,671 Mesagraecia bicolor 0 Conocephalinae 0,230 0,707 0,222 0,597 Paroxylakis setosa 0 Conocephalinae 0,254 0,804 0,220 0,724 Pyrgocorypha hamata 0 Conocephalinae 0,129 0,515 0,136 0,464 Salomona affine 0 Conocephalinae 0,217 0,802 0,202 0,699 Scytocera longicornis 0 Conocephalinae 0,203 0,971 0,185 0,756 Subria grandis 0 Conocephalinae 0,131 0,631 0,141 0,515 Acridoxena hewaniana 1 Acridoxeninae 0,328 0,297 0,702 0,311 Afromecopoda preussiana 0 Mecopodinae 0,104 0,272 0,177 0,291 Albertisiella acanthodiformis 1 Mecopodinae 0,193 0,458 0,227 0,435 Anoedopoda erosa 1 Mecopodinae 0,156 0,392 0,257 0,309 Anoedopoda lamellata 1 Mecopodinae 0,141 0,331 0,261 0,313 Biroa atrospinosa 0 Mecopodinae 0,096 0,254 0,150 0,275 Characta bituberculata 1 Mecopodinae 0,195 0,574 0,297 0,320 Euhexacentrus annulicornis 1 Hexacentrinae 0,228 0,818 0,227 0,732 Ityocephala francoisi 1 Mecopodinae 0,197 0,464 0,273 0,328 platyphoea 1 Mecopodinae 0,266 0,635 0,344 0,482 Pachysmopoda abbreviata 0 Mecopodinae 0,334 0,761 0,369 0,572 Paralistroscelis listrosceloides 0 Listroscelidinae 0,204 0,745 0,165 0,580 Parateuthras truncatus 1 Phaneropterinae 0,128 0,434 0,158 0,346 beieri 0 Hexacentrinae 0,097 0,426 0,122 0,390 Tympanophora splendida 1 Tympanophorinae 0,210 0,298 0,415 0,246 Zaprochilus mongabarra 0 Zaprochilinae 0,055 0,082 0,091 0,266 Agraecia punctata 0 Conocephalinae 0,150 0,652 0,144 0,530 Diophanes rosescens 0 Pseudophyllinae 0,219 0,640 0,264 0,644 Iaratrox maculata 0 Conocephalinae 0,147 0,509 0,145 0,491 Kevaniella bipunctata 0 Phaneropterinae 0,146 0,420 0,165 0,481 floridensis divergens 1 Pseudophyllinae 0,298 0,605 0,390 0,489 Starkonsa nigrifrons 0 Conocephalinae 0,141 0,492 0,149 0,469 Steirodon dentatum 1 Phaneropterinae 0,174 0,506 0,265 0,401 Temnophyllus atrosignatus 1 Pseudophyllinae 0,219 0,489 0,312 0,480 Temnophyllus speciosus 1 Pseudophyllinae 0,197 0,441 0,269 0,418 Trigonocorypha angustata 1 Phaneropterinae 0,162 0,884 0,214 0,575 Trigonocorypha buettikeri 1 Phaneropterinae 0,145 0,479 0,193 0,474 Trigonocorypha tiahmae 1 Phaneropterinae 0,269 0,725 0,300 0,501 Corycus sp. 1 Mecopodinae 0,361 0,612 0,541 0,462 Lesina ensifera 0 Conocephalinae 0,455 1,443 0,350 1,233 Cesacomora cucullata 1 Conocephalinae 0,413 1,335 0,339 1,007 Phaneroptera magna 0 Phaneropterinae 0,124 0,297 0,167 0,266 Phaneroptera minima 0 Phaneropterinae 0,112 0,240 0,140 0,322 Tylopsis dispar 0 Phaneropterinae 0,093 0,183 0,109 0,340 Tylopsis irregularis 0 Phaneropterinae 0,081 0,255 0,105 0,315 16

Alloteratura longicauda 0 Meconematinae 0,112 0,292 0,107 0,434 Phyllophorella inermis 1 Phyllophorinae 0,278 0,356 0,361 0,341 Phyllophorella woodfordi 1 Phyllophorinae 0,342 0,528 0,406 0,466 Sasima amplifolia 1 Phyllophorinae 0,276 0,399 0,459 0,321 Permotettigonia gallica A ? ? 0,373 1,395 0,477 0,750 Permotettigonia gallica B ? ? 0,359 1,337 0,426 0,715 Archepseudophylla fossilis ? ? 0,300 2,528 0,392 0,391 17

Supplementary table 1. Dataset for the morphometric analyses. Permotettigonia gallica

A: linear extrapolation; Permotettigonia gallica B: circular extrapolation; Mugleston et al criterion: 0: thorax height larger than FW width; 1: FW wider than thorax height; Geometry:

Anterior field circularity; ratio pf/af: posterior field width/anterior field width; Ratio W/L: width/length; Ratio afa/pfa: anterior field area/posterior field area

11 18

Comparison of two component models Models with one component Models with two components with one component models Non-leaf- Leaf-mimicking Reduction in Reduction Model SS df mimicking SS df P component AICc in BIC component Width/length Mean (A3): 50512 25 Weight (A5): 0.66 Weight (1-A5): 0.34 7074 249 >0.999 489 475 ratio 0.32 1 Mean (A3): 0.22 Mean (A1): 0.55 9 SD (A4): 0.20 SD (A4): 0.09 SD (A2): 0.07

Posterior / Mean (A3): 44754 25 Weight (A5): 0.47 Weight (1-A5): 0.53 3687 249 >0.999 623 609 Anterior field 0.44 1 Mean (A3): 0.44 Mean (A1): 1.05 9 width ratio SD (A4): 0.15 SD (A4): 0.15 SD (A2): 0.44

Anterior / Mean (A3): 47054 25 Weight (A5): 0.66 Weight (1-A5): 0.34 2434 249 >0.999 741 727 posterior field 0.42 1 Mean (A3): 0.42 Mean (A1): 0.90 9 area ratio SD (A4): 0.13 SD (A4): 0.13 SD (A2): 0.32

Anterior field Mean (A3): 54819 25 Weight (A5): 0.68 Weight (1-A5): 0.32 8327 249 >0.999 469 455 circularity 0.16 1 Mean (A3): 0.16 Mean (A1): 0.41 9 SD (A4): 0.06 SD (A4): 0.06 SD (A2): 0.06

Supplementary table 2. Comparison of non-linear regression models. Model with one

component (equation 1) compared to model with two components (equation 2) with the mean

(A1) fixed to the value obtained for the Pterochrozinae, epitomizing leaf-mimicking katydids.

SS: sum of squares; df: degree of freedom; P: probability that the data are better described

with the two component model; dAICc: difference in corrected Akaike information criterion

between the two models (decrease in AICc with two components model); dBIC: difference in

Bayesian information criterion between the two models (decrease in BIC with two

components model).

12 19

Modeling with modern katydids Measurements fossil Comparison fossil / modeling

% of non-

leaf- % of leaf- Non leaf Leaf mimicking Linear Circular mimicking mimicking mimicking component extrapolation extrapolation distribution distribution ≤ fossil component ≥ fossil value

value

Width/length Weight Weight (1-A5): ratio (A5): 0.66 0.34

Mean (A3): Mean (A1): 0.55 0.1 % - 0.8 0.48 0.43 5 % - 16 % 0.22 SD (A2): 0.07 %

SD (A4):

0.09

Posterior / Weight Weight (1-A5):

Anterior field (A5): 0.47 0.53 width ratio Mean (A3): Mean (A1): 1.05 0.72 0.72 3 % 23 % 0.44 SD (A2): 0.44

SD (A4):

0.15

Anterior / Weight Weight (1-A5): posterior field (A5): 0.66 0.34 area ratio Mean (A3): Mean (A1): 0.90 0.75 0.71 0.5 % - 1 % 28 % - 32 % 0.42 SD (A2): 0.32

SD (A4):

0.13

Anterior field Weight Weight (1-A5): circularity (A5): 0.68 0.32

Mean (A3): Mean (A1): 0.41 0.04 % - 0.37 0.36 19 % - 28 % 0.16 SD (A2): 0.06 0.09 %

SD (A4):

0.06

13 20

Supplementary table 3. Comparison of measurements taken on Permotettigonia gallica and modeling of modern katydid wings. The parameters obtained with nonlinear regression

(A1-A5) correspond to the parameters given in Equation 2.

SUPPLEMENTARY NOTES

Supplementary Note 1 | Locality and horizon

The fossil was discovered by one of us (P.R.) in the Dôme du Barrot, 760 m alt., in the Cians

Formation (Red Permian), Roua valley, near the village of Daluis, close to Var River, Alpes

Maritimes, France (Supplementary Fig. 1). It is the third fossil insect found in this Formation.

The first one is a griffenfly (Odonatoptera: Meganeuridae) (Collet du Brec, Léouvé)1-2. The second one is an undetermined insect also found at the Collet du Brec3. One of us (R.G.) has discovered in 2015 some Notostraca, Ostracoda, and arthropod ichnites in the Collet du Brec area, otherwise very poor in fossils. The Cians Formation is of continental origin constituted of red mudstones and sandstones issued from the erosion of the Variscan relief4. A Wordian or Roadian age (269-265 Ma) was proposed for the Léouvé Formation, which is above the

Cians Formation3,5. More recently, a Roadian age (272.5-268 Ma) was proposed for the red

Permian of the Dome de Barrot6.

Supplementary Note 2 | Systematic Paleontology: Extended descriptions and comments

Since all taxa are monotypic, the included species and genus are automatically herein designated as the type species and type genus for the associated generic and familial names.

Insecta Linné, 1758

Orthoptera Olivier, 1789

Ensifera Chopard, 1920

Tettigonioidea Krauss, 1902

14 21

Family Permotettigoniidae Nel et Garrouste, fam. nov.

Genus Permotettigonia Nel et Garrouste, gen. nov.

Permotettigonia gallica Nel et Garrouste, sp. nov.

2007 ‘archaeorthoptère de l'ordre des Titanoptera’ (O. Béthoux, pers. comm.)3

Holotype. MNHN-LP-R 63853, Muséum National d’Histoire Naturelle, Paris, France.

Etymology. The genus name refers to Permian and Tettigonia; the species name refers to the

Latin name for France.

Diagnosis. The fossil is a nearly complete and very broad tegmen (fore wing) with a very broad corrugate field between subcostal vein ScP and anterior wing margin, crossed by numerous long veinlets alternatively convex and concave, all nearly perpendicular to ScP and to anterior wing margin. A second broad field is present between radial vein R and median vein M, and a third between M and cubital complex vein CuA+CuPaα; all crossed by long veinlets more or less curved and perpendicular to main longitudinal veins; M and

CuA+CuPaα simple and distally fused again; CuP divided into branches CuPaα, CuPa, and

CuPb.

Description. This fossil is the imprint in rock of the antero-basal part (ca. four-fifth of wing) of a fore wing; no trace of coloration preserved; it is impossible to determine whether it is a right or left wing. Length of fragment 33.0 mm, width 15.0 mm; probable length of wing ca.

40 mm; presence of an enigmatic zone near bases of radius and ScP that could correspond to costal field between a possible vein ScA and costal margin, rather short and broad, 7.0 mm long, 3.0 mm wide, with phantom-like traces of veins; concave vein ScP closely parallel to convex R (distally RA), diverging near their apices; field between ScP and anterior wing margin very broad and long, 26.0 mm long, 5.5 mm wide, crossed by a series of about 26 alternatively concave and convex veins, all straight, and nearly perpendicular to ScP and anterior wing margin, distance between two such concave veins ca. 2 mm; presence of

15 22 parallel longitudinal short crossveins present between these veinlets, defining small quadrangular cells; RP emerging from R far from wing base, simple in its preserved part, making a deep posterior curve and directed distally towards RA; presence of a secondary longitudinal vein between RP and RA, not directly branching on RA; M+CuA separating from radius near wing base; a broad and elongate field between R and M, 25.0 mm long, 4.0 mm wide, crossed by a series of long veinlets more or less perpendicular to R and M and a rather irregular archedictyon between these veinlets; concave M and convex CuA separated ca. 2.0 mm from wing base; an elongate and narrow field between M and CuA, 18.0 mm long,

3.0 mm wide; M and CuA fused again 24.0 mm from wing base; concave CuP divided into two branches CuPa and CuPb near wing base; CuPa separating into CuPaα and CuPa ca. 5 mm distal of wing base; CuPaα short and ending on CuA; CuPa and CuPb simple and nearly straight; a simple and straight first anal vein posterior to CuPb, other anal veins not preserved or absent; field of CuP – anal vein very narrow and reduced compared to the rest of the wing, ca. 14 long and 2 mm wide, nearly perpendicular to the main plan of the wing surface.

Discussion. The pattern of venation of Permotettigonia corresponds to that of an Orthoptera in the basally fused veins R, M and CuA, presence of M+CuA, CuP with two main branches

CuPb and CuPa, the latter being subdivided into a short CuPaα distally ending into CuA, and a long CuPa7. Permotettigonia displays all the synapomorphic characters of the

Tettigoniidae, i.e., complete absence of the vein MA, M and CuA with no secondary branches; archedictyon always present, but more or less developed8. Permotettigonia differs from the modern Tettigoniidae in the presence of a CuP subdivided into branches CuPa,

CuPa, and CuPb, while the latter have a CuPa distally forked or not, and no CuPb

(apomorphy of the modern katydids) (see Fig. 1, Supplementary Fig. 2), the situation in

Permotettigonia being then plesiomorphic7. Permotettigonia is not a representative of the crown group Tettigoniidae, but certainly belongs to the stem group of the Tettigoniidae. The

16 23 type tegmen of Permotettigonia shows no trace of stridulatory organ, suggesting it could be that of a female, or a mute male.

Supplementary Note 3 | Remarks

1) Few Paleozoic and Mesozoic Orthoptera have a broad subcostal field with a series of veinlets nearly perpendicular to ScP and costal margin:

- The Mesozoic Deinovitimia insolita Gorochov, 1989 (in the enigmatic family Vitimiidae

Sharov, 1968). This taxon differs from Permotettigonia in the pectinate MP+CuA and the forked RP(+MA)8-9;

- The Middle Permian Raphogla rubra Bethoux et al., 2002 (in the enigmatic family

Raphoglidae Bethoux et al., 2002). This taxon differs from Permotettigonia in the MP+CuA,

MA, and RP with several branches10.

2) The Lower Cretaceous Haglotettigonia Gorochov, 1988 is, after Gorochov11, the oldest representative of the Tettigonioidea, and unique representative of the extinct

Haglotettigoniidae. Gorochov12 justified the affinities of this taxon with the Tettigoniidae on the basis of the following characters (translated from the Russian by our colleague Alexander

Kirejtshuk): ‘fore wing of male of primitive structure, mostly similar to Hagloidea; stems Sc and R placed apart each other; there are remains of distal part of second branch of МА and also completely developed, but broken CuA2 with distal and proximal parts shifted relatively each other along diagonal vein; diagonal vein developed, angularly curved and with pectinate fan; between the base of distal part of CuA2 and diagonal vein there is somewhat widened cell (precursor of mirror of Tettigoniidae); strings well expressed; MP+CuA1 clearly pectinate; transverse venation normal, i.e. not transformed into a net of secondary archedictyon. These characters distinguish the new family from Tettigoniidae’.

17 24

Among these characters, only the cell ‘precursor’ of the mirror of Tettigoniidae would support an affinity with this family because all other characters are plesiomorphies. The problem is that Haglotettigonia has no real wide cell that could be considered as a mirror but a net of rather small cells in the field where the alleged mirror should be12. Consequently the affinities of Haglotettigonia with the Tettigoniidae should be verified.

3) The modern caeliferan Trigonopterygidae have also leaf-like tegmina, with several specializations convergent with the leaf-like katydids, viz. the presence of a double longitudinal vein that mimics the median vein of an angiosperm leaf, presence of a very broad subcostal field, etc. Nevertheless these Caelifera strongly differ from our fossil in the median vein that becomes fused again with radius in basal third of tegmina, and RP that is joined to

RA for a long distance and emits several posterior branches before separating from RA.

SUPPLEMENTARY REFERENCES

1. Laurentiaux-Vieira, F. & Laurentiaux, D. Découverte d'un insecte protodonate dans le

Permien des Alpes Maritimes. Comptes-Rendus de l'Académie des Sciences 257,

3018-3020 (1963).

2. Nel, A. et al. Revision of Permo-Carboniferous griffenflies (Insecta: Odonatoptera:

Meganisoptera) based upon new species and redescription of selected poorly known

taxa from Eurasia. Palaeontographica (A) 289, 89-121 (2009).

3. Durand, M. & Gand, G. Le Permien et le Trias du Dôme de Barrot (Alpes-Maritimes).

Livret-guide de l’excursion annuelle de l’Association des Géologues du Permien et du

Trias, 18-20 septembre 2007: 1-26 (2007).

18 25

4. Bourquin, S., Durand, M., Diez, J.B., Broutin, J. and Fluteau, F. 2007. The Permian-

Triassic boundary and lower Triassic sedimentation in western European basins: an

overview. Journal of Iberian Geology, 33 (2): 221-236.

5. Kruiver, P. P. et al. The implications of non-suppressed geomagnetic secular variation

during the Permo-Carboniferous Reversed Superchron. Physics of the Earth and

Planetary Interiors 131, 225-235 (2002).

6. Haldan, M.M. et al. A comparison of detailed equatorial red bed records of secular

variation during the Permo-Carboniferous Reversed Superchron. Geophysical Journal

International 177, 834-848 (2009).

7. Béthoux, O. & Nel, A. Venation pattern and revision of Orthoptera sensu nov. and

sister groups. Phylogeny of Palaeozoic and Mesozoic Orthoptera sensu nov. Zootaxa

96, 1–88 (2002).

8. Gorochov, A. V. [New taxa of the orthopteran families Bintoniellidae, Xenopteridae,

Permelcanidae, Elcanidae and Vitimiidae (Orthoptera, Ensifera).] Vestnik Zoologii 27,

20-27. [in Russian.] (1989).

9. Gorochov, A. V. Sistema i evolyutsiya pryamokrylykh podotryada Ensifera

(Orthoptera) [System and Evolution of the suborder Ensifera (Orthoptera).] Parts 1

and 2. Trudy Zoologicheskogo Instituta 260, 3-224 & 261, 3-212. [in Russian] (1995).

10. Béthoux, O. et al. Raphogla rubra gen. n., sp. n., the oldest representative of the clade

of modern Ensifera (Orthoptera: Tettigoniidea, Gryllidea) (Lodève Permian basin,

France). European Journal of Entomology 99, 111-116 (2002).

11. Gorochov, A. V. Review of Triassic Orthoptera with descriptions of new and little

known taxa: part 2. Paleontological Journal 39, 272-279 (2005).

12. Gorochov, A. V. [Classification and phylogeny of katidids (Gryllida = Orthoptera,

Tettigonioidea).] pp. 145-190. In: Ponomarenko, A. G. (ed.). Melovoj biotsenoticheskij

19 26

krizis i evolutsiya nasekomykh. [Cretaceous biocoenotic crisis and insect evolution.],

Nauka, Moscow, 1-230 [in Russian.] (1988).

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