A complete insect from the Late Devonian periodRomain Garrouste1, Gael Clement2, Patricia Nel1, Michael S. Engel3, Philippe Grandcolas1, Cyrille D’Haese1, Linda Lagebro4,Julien Denayer5, Pierre Gueriau2,6, Patrick Lafaite7, Sebastien Olive5,8, Cyrille Prestianni8 & Andre Nel1
After terrestrialization, the diversification of arthropods andvertebrates is thought to have occurred in two distinct phases1,the first between the Silurian and the Frasnian stages (LateDevonian period) (425–385 million years (Myr) ago), and the sec-ond characterized by the emergence of numerous new major taxa,during the Late Carboniferous period (after 345 Myr ago). Thesetwo diversification periods bracket the depauperate vertebrateRomer’s gap (360–345 Myr ago) and arthropod gap (385–325 Myrago)1, which could be due to preservational artefact2,3. Although arecent molecular dating has given an age of 390 Myr for theHolometabola4, the record of hexapods during the Early–MiddleDevonian (411.5–391 Myr ago, Pragian to Givetian stages) is excep-tionally sparse and based on fragmentary remains, which hindersthe timing of this diversification. Indeed, although DevonianArchaeognatha are problematic5,6, the Pragian of Scotland has givensome Collembola and the incomplete insect Rhyniognatha, with itsdiagnostic dicondylic, metapterygotan mandibles5,7. The oldest,definitively winged insects are from the Serpukhovian stage (latestEarly Carboniferous period)8. Here we report the first complete LateDevonian insect, which was probably a terrestrial species. Its‘orthopteroid’ mandibles are of an omnivorous type, clearly notmodified for a solely carnivorous diet. This discovery narrows the45-Myr gap in the fossil record of Hexapoda, and demonstrates
further a first Devonian phase of diversification for the Hexapoda,as in vertebrates, and suggests that the Pterygota diversified beforeand during Romer’s gap.
The insect was recovered from the Famennian Strud locality,Namur province, Belgium (50u 269 43.3299 N, 5u 039 24.8699 E), knownwidely for its early tetrapods9,10. It was found in a freshwater asso-ciation including plants11, numerous Crustacea (Branchiopoda andMalacostraca) and Chelicerata (Eurypterida) (Fig. 1, SupplementaryFigs 1 and 2 and Supplementary Information 1). The specimen iscomprised of a two-dimensional compression with median abdominalstructures elevated owing to natural filling of the gut, and excludes thepossibility that the material represents an exuvia. A ‘shadow’ of organicorigin surrounds the body. The connections of the appendages withthe body are partly destroyed because of a well-known compressionand decay process12, rendering difficult the study of some parts. Theappendages were not displaced, except for one or two legs.
Class InsectaClade Dicondylia
Strudiella devonica gen. et sp. nov.
Etymology. Strudiella is a diminutive form based on the type localityStrud (the name is feminine); devonica is after the Devonian age of thefossil.
1UMR CNRS 7205, CP 50, Entomologie, Museum national d’Histoire naturelle, 45 rue Buffon, F-75005 Paris, France. 2UMR CNRS 7207, Paleontologie, Museum national d’Histoire naturelle, 8 rue Buffon,F-75005 Paris, France. 3Division of Entomology, Natural History Museum, and Department of Ecology and Evolutionary Biology, 1501 Crestline Drive – Suite 140, University of Kansas, Lawrence, Kansas66045, USA. 4Department of Earth Sciences, Uppsala University, Villavagen 16, SE-752 36 Uppsala, Sweden. 5Service de Paleontologie animale et humaine, Departement de Geologie, Universite de Liege,Bat. B.18, Allee du Six-Aout, Sart Tilman, B-4000Liege, Belgium. 6IPANEMA,USR 3461CNRS- Ministere de la Culture etde la Communication, F-91190,Saint-Aubin, France. 7CNRS– MNHN DICAP,ServiceMultimedia, CP 27, 57 rue Cuvier, F-75005 Paris, France. 8Royal Belgian Institute of Natural Sciences Paleontology Department, 29, Rue Vautier, B-1000 Brussels, Belgium.
Malacostraca
Conchostraca
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Figure 1 | Partial Strud stratigraphy (fossiliferous levels), Bois des Mouches Formation, Upper Famennian.
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Holotype. IRSNB a12818a–b, part and counterpart, by presentdesignation.Diagnosis and description. Apterous, body elongate and narrow,8.0 mm long and 1.7 mm wide (Fig. 2a, b); six thoracic, uniramouslegs with tibiae and femora long and thin; antenna uniramous (Figs 2aand 3a), long, with scape and pedicel distinctly broader than remainingantennomeres, about 10 short flagellomeres; mandible triangular (ofmetapterygotan form) with a continuous series of sharp but smallirregular molar and incisor cusps (Fig. 3b, c and Supplementary Fig. 3);large dark eyes in posterior part of head; head rather small; thoraxbroad, well separated from head and abdomen, with a rounded struc-ture covering posterior half of head, corresponding to an expanded
pronotum; abdomen divided into 10 segments, without lateral leglets,gills or other appendicular structures.
The presence of a thorax separated from the head and abdomen,bearing three pairs of legs, is one of the hallmark apomorphies of theHexapoda13. Further features of significance are long, uniramous legs,one pair of long, uniramous antennae, large eyes, abdomen dividedinto 10 segments and absence of abdominal leglets. Although thesecan be found individually in different crustacean clades14,15, their com-bination with the aforementioned apomorphy of hexapods is distinctlyinsectan and precludes an interpretation of this fossil as a juvenileNotostraca, which are abundant in the layer (see SupplementaryInformation). The scape and pedicel being distinctly broader than
b
abd
md ant
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Figure 2 | General habitus of Strudiella devonica gen. et sp. nov. a, Photograph of the part. b, Reconstruction of general habitus. Scale bar, 1 mm. White arrowsindicate legs visible on part. abd, abdomen; ant, antenna; h, head; md, mandible.
md
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Figure 3 | Strudiella devonica gen. et sp. nov., counterpart details.a, Photograph of anterior part of head. b, Photograph of left mandible.c, Reconstruction of left mandible. Scale bars, 0.45 mm (a), 0.2 mm (b),
0.1 mm (c). 3rd S, third antennal segment; ey, eye; md, mandible; p, maxillarypalp; pe, pedicel; Sc, scape.
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the distal segments constitute a synapomorphy of the Insecta withinthe Hexapoda, related to the presence of muscles and Johnstonorgan13–16. The first two antennal segments being larger than the othersis a character also present in Chilopoda, especially lithobiomorphs;however, the combination of characters does not match attribution toMyriapoda. Among the Hexapoda, the long femora and tibiacorrespond to those found among pterygotes, rather than those of thewingless Archaeognatha or Zygentoma17. Within the Pterygota, themandibles are of an ‘orthopteroid’ type, short and triangular6,18–22, andcurrently considered an apomorphy of the winged Metapterygota(Pterygota, excluding Palaeodictyoptera and Ephemeroptera)5,6,18,19.Unfortunately, wings are not observable on the present specimen.The absence of wings plus the minute size suggests that the individualwas a nymph, but a conclusive determination about the absence ofgenital structures cannot be established owing to the poor preser-vation of the abdominal apex.
The expanded pronotum is similar to those of many insect lineages(for example, Dictyoptera and Grylloblattodea), and its presence in aMiddle-Palaeozoic-era insect is not surprising. The lack of lateralappendages (leglets and gills) on the abdominal segments is clearlyderived relative to the condition in the wingless Zygentoma, anddiffers from nymphs (but not adults) of several pterygote orders,although whether these are individually derived in those immaturesor are plesiomorphic is debatable23. Strudiella shares, with themost basal hexapod lineages, antennae with uniformly similarflagellomeres5,15,24.
The long legs without adaptations for swimming, plus the apparentabsence of abdominal gills and rarity of Strudiella within the arthropodfauna of the Strud locality, support the hypothesis that it was a terrestrialanimal. It must have been omnivorous or phytophagous but certainlynot carnivorous given the weak development of the incisor comparedwith the molar cusps, and the sharp irregular cusps corresponding tothe ‘omnivorous type’ of Gangwere25. Strudiella and Rhygniognathacertainly had different feeding habits as the mandibles of
Rhygniognatha had sharper cusps, corresponding to mycetophagyand/or saprophagy but not to carnivory26.
Ward et al.1 supposed that the Early Carboniferous low oxygeninterval corresponding to the Romer’s gap (360–345 Myr ago) con-strained the timing of diversification of the Hexapoda as well as for otherarthropods. The high morphological disparity of the pterygote insects inthe Serpukhovian stage (320 Myr ago), now well documented7,27,suggests that the diversification of this clade occurred very rapidly afterRomer’s gap, or more likely during it, in accordance with the recentdiscoveries of early Carboniferous terrestrial arthropods2. Strudiellademonstrates further that an early diversification of the dicondylicinsects occurred before Romer’s gap4 (Fig. 4), well in accordance withthe presence of a diversified abundant terrestrial vegetation, includingforests, since the mid-Devonian6,11,28–30.
METHODS SUMMARYThe material is housed at the Royal Belgian Institute of Natural Sciences (Brussels,Belgium). The fossils were prepared using a sharp knife. Photographs were takenusing an Olympus SZX9 stereomicroscope system with an Olympus E3 digitalcamera, and the fossil was moistened with 70% alcohol. Illustrations were preparedusing a camera lucida on a binocula Olympus SZX9.
Received 3 April 2012; accepted 1 June 2012.
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Time (Myr)
Silurian DevonianSilurian DevonianMississipian
Permian
Pennsylvanian
Carboniferous
Cisuralian Guadal. Loping.
Entognatha
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Zygentoma
Strudiella
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Ephemeroptera
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Figure 4 | Phylogeny of basal hexapod clades. Hexapoda gap in dark grey, Romer’s gap in pale grey, (411.5 Myr ago); Rhyniella praecursor (1) Hirst and Maulik,1926; Rhyniognatha hirsti (2) Tillyard, 1928; undescribed fossil (3) from Gilboa (391 Myr ago). {, no extant lineages.
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Supplementary Information is linked to the online version of the paper atwww.nature.com/nature.
Acknowledgements We thank O. Bethoux who discovered and prepared most of thearthropodmaterial fromStrud including the specimendescribed herein. We also thankG. Budd and G. Edgecombe for discussion on the fossil material and improving the firstversion of the paper, Gesves local council staff and field workers of the Strudexpeditions,G.Odebert andS. Fernandez forpreparing illustrations, andC. Lemzaoudaand O. Bethoux for photographs of the associated arthropod fauna. Thanks are due toA. Folie for our request of a catalogue number for the specimen described herein(requests for materials can be sent to [email protected]). This work was partlysupported by the French National Agency under the TERRES project (numberANR-2010-BLAN-607). Support for M.S.E. was provided by US National ScienceFoundation grant DEB-0542909.
Author Contributions R.G., P.N. and G.C. are first authors with equal rank; R.G., A.N.,P.N., P.G., C.D’H., L.L., M.S.E., J.D., C.P., P.G. and S.O. drafted the manuscript andprepared figures. A.N. and P.N. coordinated the manuscript; G.C. coordinated andparticipated in fieldwork at the Strud locality and contributed to the draft manuscript;L.L., J.D., C.P., P.G. and S.O. also participated in fieldwork.
Author Information Reprints and permissions information is available atwww.nature.com/reprints. The authors declare no competing financial interests.Readers are welcome to comment on the online version of this article atwww.nature.com/nature. Correspondence and requests for materials should beaddressed to R.G. ([email protected]) or A.N. ([email protected]).
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