Saturday 4 December 2021

Ctenoptilus frequens and the first appearance of Orthopteran Insects.

The first Insect faunas appeared in the early Late Carboniferous, around 307 million years ago. These faunas included a range of Insect groups, including the Griffenflies (early relatives of the modern Dragonflies and Damselflies), the Megasecopterans, an extinct group of Insects interpreted as being sap-feeders, and the Lobeattids and Cnemidolestods, interpreted as extinct relatives of the Orthopterans (Crickets, Grasshoppers, etc.).

The Lobeattids are usually interpreted as either stem-group Orthopterans; i.e. Insects more closely related to Orthopterans than to any other extant group, but not descended from the most recent common ancestor of all living Orthopterans (which is thought to have lived after them anyway), or more distantly related members of the Polyneoptera (the group which includes Orthopterans, Blatoids, and Earwigs, as well as some smaller extant groups and several extinct orders of Insects). The exact relationship of Lobeattids to modern Insect groups is hard to determine without examples of wings from the Early Carboniferous (or earlier).

In a paper published in the journal eLife on 30 November 2021, Lu Chen of the College of Life Sciences and Academy for Multidisciplinary Studies at Capital Normal University, Jun-Jie Gu of the Institute of Ecological Agriculture at Sichuan Agricultural University, Dong Ren, also of the College of Life Sciences and Academy for Multidisciplinary Studies at Capital Normal University, Alexander Blanke of the Institute of Evolutionary Biology and Animal Ecology at the University of Bonn, and Olivier Béthoux of the Centre de Recherche en Paléontologie de Paris at Sorbonne Université, and the Muséum National d’Histoire Naturelle, present the results of a study which examined the Lobeattid Insect Ctenoptilus frequens, from the 307-million-year-old Yanghugou Formation of the Ningxia Hui Autonomous Region in China.

The Yanghugou Formation outcrops at Xiaheyan in Zhongwei City. It has yielded a high number of Insect fossils which preserve a great deal of detail, enabling detailed studies of the anatomy of extinct Insect groups. Of these, several hundred specimens of a new species of Lobeattid Insect, named Ctenoptilus frequens because of its high abundance, have been recovered. These specimens form the basis of Chen et al.'s study.

Ctenoptilus frequens, holotype (CNU-NX1-326). (A) Habitus drawing and (B) habitus photograph (composite); (C)–(D) details of head and right foreleg (location as indicated in (B)), (C) color-coded interpretative drawing and (D) photograph (composite); and (E)–(F) details of ovipositor (location as indicated in (B)), (E) drawing and (F) photograph (composite). Colour-coding and associated abbreviations: red, lacina (la); dark blue-purple, mandible (md); green, pharynx (pha). Other indications, head: ce, composite eye; f, frons; co, coronal cleavage line; fc, frontal cleavage line. Wing morphology abbreviations: LFW, left forewing; LHW, left hind wing; RFW, right forewing; RHW, right hind wing; ScP, posterior subcosta; RA, anterior radius; RP, posterior radius; M, media; CuA, anterior cubitus; CuPa, anterior branch of posterior cubitus; CuPb, posterior branch of posterior cubitus; AA, anterior analis. Chen et al. (2021).

All Insect ovipositors have a series of valves, made up of a pair of mesal extensions, the gonopods, or ovipositor blades, and a pair of lateral projections, the gonostyli, or ovipositor sheaths on the eighth and ninth abdominal segments. In Ctenoptilus frequens these are heavily sclerotised, and form three pairs of valves, with boundaries at the dorsal margin of the gonostylus IX, the ventral margin of the gonapophysis IX, and the dorsal and ventral margins of gonapophysis VII. Also present is a a thin longitudinal line much sharper and more developed than other visible linear structures, which appears from the second third of their length onwards. This is interpreted as the primary olistheter, a tongue-like structure which commonly interlocks with the ventral margin of the gonapophysis IX and the dorsal and ventral margins of gonapophysis VIII.

External ovipositor in Ctenoptilus frequens in lateral view. (A)–(C) Specimen CNU-NX1-749, (A) overview of the ovipositor with overlaid indications of the ovipositor parts (see also) overview of the ovipositor with overlaid indications of the ovipositor parts. (B) composite photograph and (C) reflectance transforming imaging (RTI) extract in normal visualisation; (D)–(F) specimen CNU-NX1-742, (D) overview of the ovipositor with overlaid indications of the ovipositor parts overview of the ovipositor with overlaid indications of the ovipositor parts; (E) composite photograph and (F) RTI extract in normal visualisation. Olistheter (‘olis’) configurations at different parts of each respective ovipositor are shown as insets. Abbreviations: Gonostylus IX (gs9); gonapophysis IX (gp9); gonapophysis VIII (gp8). Chen et al. (2021).

Combined with the position of the antero-basal apophysis (outgrowth) this enables the determination of the anterior margin of the gonapophysis IX, which appears to reach the apex of the ovipositor, although the dorsal margin of this valve could not be determined. The gonapophysis VIII bears a number of teeth, orientated ventrally, and more numerous towards the apex. 

Ctenoptilus frequens, specimens composed of body remains including well-preserved head, legs, and/or ovipositor. (A)–(E) Specimen CNU-NX1-749; (A) photograph of habitus (composite), left forewing as positive imprint; (B)–(C) details of ovipositor (location as indicated in (A)), polarity unclear, (B) drawing and (C) photograph (composite); and (D)–(E) details of head (location as indicated in (A)), (D) colour-coded interpretative drawing and (E) photograph (composite). (F)–(H) Specimen CNU-NX1-756; (F) photograph of habitus (composite); and (F)–(H) details of head (location as indicated in (F)), imprint polarity unclear, (G) colour-coded interpretative drawing (F) photograph (composite). (I)–(K) Specimen CNU-NX1-754; (I) photograph of habitus (composite), (J)–(K) details of distal portions of fore-legs and a mid-leg (location as indicated in (I)), (J) drawing and (K) photograph (composite). Chen et al. (2021).

This implies that only the gonostylus IX and gonapophysis IX extend dorsally beyond the gonapophysis VIII, and that the longitudinal line seen dorsal to the ventral margin of the gonapophysis IX must be a second olistheter which interlocks with these valves; this is supported by these valves remaining locked together in even quite badly decayed specimens. 

Ctenoptilus frequens, specimen CNU-NX1-742. (A) Photograph of habitus (composite), right forewing as positive imprint, flipped horizontally, and (B)–(C) details of ovipositor (location indicated in (A)). Photograph of habitus (composite), right forewing as positive imprint, flipped horizontally, and (B)–(C) details of ovipositor (location indicated in (A)), (B) drawing and (C) photograph (light-mirrored). Chen et al. (2021).

The presence of a second olistheter in Ctenoptilus frequens places the species firmly within the Orthoptera. This is a trait found in the modern Ensifera (Crickets), one of the two major subdivisions of the Orthoptera, and absent in the other, the Caelifera (Grasshoppers). This implies that either Ctenoptilus frequens is a crown-group Orthopteran (i.e. a descendent of the last common ancestor of all living Orthopterans) more closely related to the Ensifera than the Caelifera, or that it is a stem group species, and that the second olistheter has been secondarily lost in the Caelifera.

The evolution of major ovipositor configurations across Orthoptera. (A) External ovipositor of external ovipositor of Ceuthophilus sp. (Orthoptera: Rhaphidophoridae; extant species) in laterial view (left side, flipped horizontally, left gonostylus IX (gs9) removed). (B) Same as above, but annotated. The three black vertical lines labelled ‘a’, ‘b’, ‘c’ indicate the position of the three schematic sections shown in (C). (C) Schematic ovipositor cross-sections in Grylloblattodea, Ctenoptilus frequens, and several extant Orthoptera possessing well-developed ovipositors (not to scale). Pale cross-section along the stem of Grylloidea is hypothetical; sections delineated by brackets represent conditions along the antero-posterior axis. Color-coding and associated abbreviations: light blue, gonostylus IX (gs9; light green, gonapophysis IX (gp9); red, gonapophysis VIII (gp8); royal blue, secondary olistheter (olis2); light orange, tertiary olistheter (olis3); purple, ‘lateral basivalvular sclerite’ (specific to Caelifera). Other indications: olis1, primary olistheter; int./ext., internal/external, respectively; dors./ventr., dorsal/ventral, respectively; and ant./post., anterior/posterior, respectively. Chen et al. (2021).

One of the traits that currently defines the crown-group Orthoptera is the presence of an enlarged pair of hind legs, with specialist adaptations for jumping. Another is the presence of a fork on the CuPa wing-vein before its fusion with the CuA vein, something also present in stem-group species thought to be close to the crown-group. Both of these traits are absent in Ctenoptilus frequens, making it unlikely that the species is a member of the crown-group. Chen et al. therefore suggest that Ctenoptilus frequens and other Lobeattid Insects should be regarded as stem-group Orthopterans, and that the loss absence of a second olistheter in the Caelifera is the result of a secondary loss of this trait.

The evolutionary differentiation of the Ensifera and Caelifera is not really possible to determine from extant species, and while previous fossils have been used to suggest an Ensifera-like Orthopterans-first scenario, the exact taxonomic status of those fossils was unclear, leading to a low level of confidence in the model. The excellent preservation and numerous specimens of Ctenoptilus frequens allow for a much better understanding of its anatomy and therefore taxonomic placement, strongly supporting the idea that it is a stem-group Orthopteran with an Ensiferan-like ovipositor. Since placing a member of a stem-group within the Ensifera would clearly be unhelpful taxonomically, Chen et al. suggest the creation of a new taxon, the Neoclavifera, which should include all stem-group Orthopterans with a Ensiferan-like ovipositor, plus all crown-group Orthoptera, including those which have secondarily lost this trait.

The great abundance of the Lobeattid Insects in all Late Carboniferous deposits where Insect faunas are preserved, suggests that these proto-Orthopterans were a major component of ecosystems at this time, and that they underwent a major diversification event early in the history of Insects as a whole.

Modern Orthopterans lay their eggs in a variety of environments, but the majority deposit their eggs in shallow soil. This is particularly true for the Ensifera who use their long ovipositors to puch eggs into the ground, although some species insert their eggs within Plant tissues. However, those species which lay their eggs in Plant tissues have adaptations for this specialisation which are absent in Ctenoptilus frequens, supporting the theory that this species laid its eggs in the ground, and that this is most likely the original state within the Orthoptera.

Reconstruction of a female of Ctenoptilus frequens laying eggs. Xiaoran Zuo in Chen et al. (2021).

Leaf damage from Insect feeding is very common in modern tropical forests, with many Insect groups producing distinctive feeding traces. In contrast, feeding traces on Carboniferous leaf-fossils are actually quite rare, and generally restricted to margin and hole feeding on the leaves of Pteridosperms. This damage is often attributed to stem-group Orthopterans, the descendants of which produce such damage today. However, Chen et al. question this, as the rarity of this type of damage does not appear to fit well with the great abundance of these Insects. They suggest that the mouthparts of Ctenoptilus frequens make it likely that this species was an opportunistic omnivore rather than a specialist leaf-eater, and that if this was true for other Lobeattids, then this would explain the difference between the ubiquitousness of these Insects, and the low level of leaf-feeding in the Plant communities that sustained them.

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