Fossil Friday: The Carboniferous Explosion of Winged Insects
Among the numerous abrupt appearances of new animal body plans in the history of life (Bechly 2024) there are also striking examples from my own field of research, which is the fossil history of winged insects (Pterygota), the most diverse group of organisms which includes more described species than all other multicellular life combined (Grimaldi & Engel 2005). Therefore, this Fossil Friday features the holotype of Fouquea superba, a winged insect of the order Palaeodictyoptera from the Upper Carboniferous of Commentry in France.
There have been three key innovations in the history of insects that contributed to the great success of this group. Those include the origin of wings and flight, the origin of foldable wings (Neoptera), and the origin of complete metamorphosis (Holometabola) (Nicholson et al. 2014). It is truly astonishing that all these three innovations appeared abruptly and very early among the oldest winged insects from the Carboniferous, which also exhibited a great diversity and disparity from the very beginning. I call this the Carboniferous Insect Explosion.
In the Pennsylvanian (Upper Carboniferous) subperiod between 323-299 million years ago, when the world was forming a single supercontinent Pangaea dominated by vast tropical swamp forests, this large diversity of different winged insect groups appeared suddenly without any known transitional forms in the older Mississippian (Lower Carboniferous) or Devonian strata (Strahler 1999, Labandeira 2005, Grimaldi & Engel 2005, Knecht et al. 2011, Nicholson et al. 2015, Wang et al. 2016, Bechly 2023a). According to leading experts, “an insect equivalent of an Archaeopteryx remains elusive” (Grimaldi & Engel 2005: 160).
The early fossil record of Carboniferous winged insects does not only include giant palaeopteran insects like the extinct palaeodictyopterids, mayflies, and dragonflies, or “primitive” neopteran insect orders like stoneflies, roaches, and orthopterans, but also thrips, bugs, and even advanced holometabolans like wasps, beetles, and scorpionflies, often with “a high degree of specialization early in the evolution of insects” (Garwood & Sutton 2010). Here is a brief and incomplete list of the large diversity of early winged insect groups in the Carboniferous with their oldest known representatives (also see Nel et al. 2013: fig. 3:
Palaeodictyopterids: Delitzschala (Germany, 323 mya)
Mayflies (Ephemeroptera): Triplosoba (France, 303-299 mya)
Dragonflies / Griffenflies (Odonatoptera): Eugeropteron and Geropteron (Argentina, 325-324 mya?)
Stoneflies (Plecoptera): Gulou (China, 318-314 mya)
Roaches (Dictyoptera): Kemperala (Germany, 318 mya) and Qilianiblatta (China, 318-314 mya)
Orthopterans: Archaeorthoptera (Czech Rep., 324 mya)
Thrips (Thysanoptera): Westphalothripides (France, 314-307 mya)
Plant lice (Psocodea): Westphalopsocus (France, 314-307 mya)
Bugs (Hemiptera): Protoprosbole (Belgium, 316 mya) and Aviorrhyncha (France, 314-307 mya)
Holometabolan larvae: Metabolarva (Germany, 314-307 or 306 mya) and Srokalarva (USA, 311-307 mya)
Wasps (Hymenoptera): Avioxyela (France, 314-307 mya)
Beetles (Coleoptera): Stephanastus (France, 303-299 mya)
Neuropteroids: Srokalarva (USA, 311-307 mya) seems to be a larval neuropteroid according to Haug et al. (2015)
Scorpionflies (Mecoptera): Westphalomerope (France, 318-314 mya)
Of course, there is always considerable uncertainty concerning the identification of such fossil insects. A good example is Adiphlebia lacoana from the Pennsylvanian Mazon Creek locality in Illinois. This taxon was identified as oldest beetle by Béthoux (2009), which was accepted by Wolfe et al. (2016) and even used as fossil calibration point for the dating of beetle origins. However, the attribution of Adiphlebia to beetles was disputed by Kukalova-Peck & Beutel (2012), who instead considered it as a stem neuropterid, while it was later identified as paoliid stem dictyopteran by Kirejtshuk et al. (2014). Rasnitysn & Aristov (2013) transferred Adiphlebia to the extinct family Anthracoptilidae, which was concurred by Guan et al. (2016), who thoroughly discussed the various hypotheses for the relationship of this family (i.e., Palaeodictyopteroida, Prothorthoptera, Hypoperlida, Eoblattida (= Cnemidolestodea), stem-Mantodea, Paraneoptera, Holometabola), but ultimately supported the newer alternative of a position in Paoliida as sister group of Dictyoptera. Even though the holotype specimen of Adiphlebia is a very complete and well-preserved fossil insect, it has been attributed in the past fifteen years by different experts to almost all of the major subgroups of winged insects. Keep this in mind when you read about the next discovery of a sensational transitional fossil in the news.
Where are the Stem Pterygotes?
Given that we find so many different subgroups of modern winged insects in the Carboniferous, shouldn’t we expect to find at least some stem-pterygotes among the earliest winged insects? What and where are they? Only two candidates were suggested, namely Palaeodictyopterida and Paoliida.
Palaeodictyopteroids are an extinct group of large insects with densely veined wings and sucking-piercing mouth parts. They rank among the oldest known winged insects and were considered to be stem-pterygotes by the godfather of paleoentomology Anton Handlirsch (1906-1908), but this is no longer believed among modern experts. Their phylogenetic position is still a matter of debate, but they are generally considered to be crown group pterygotes, either more closely related to living Palaeoptera (mayflies and dragonflies) or to living Neoptera (all other winged insects, with foldable wings) (Rasnitsyn & Quicke 2002, Grimaldi & Engel 2005, Prokop & Engel 2019, Prokop et al. 2019). Prokop et al. (2019) explicitly stated that “interestingly, Palaeodictyopterida have not been recovered as sister group to all other Pterygota.” In my view, their palaeopteran wing articulation, their wing venation, their genital organs with paired penes, and larval characters with abdominal winglet-like structures (Haug et al. 2014, Prokop et al. 2022, Ross 2022), all suggest a position of palaeodictyopteroids in Palaeoptera, most likely as sister group of modern mayflies.
Paoliida are another group of early pterygote insects from the Upper Carboniferous and Permian. Based on some obsolete earlier hypotheses (Sharov 1966, Rasnitysn 1976, also see Rasnitysn & Quicke 2002), Prokop et al. (2012) considered Paoliida as “putative stem-group of winged insects”, even though Prokop & Nel (2007) had already cautioned that such a view is not supported by any synapomorphies. Consequently, no other experts accepted this hypothesis. More recent studies (Prokop et al. 2014, 2023, Legendre et al. 2015) identified Paoliida as the sister-group of roachoids (Dictyoptera) within modern Neoptera, which was also accepted and endorsed by the previous supporters of the alternative stem-pterygote hypothesis.
The only remaining potential stem-pterygote could be Carbotriplurida, which was actually suggested in a study co-authored by myself (Staniczek et al. 2014) and accepted by some later studies (e.g., Prokop et al. 2023). However, Carbotriplura from the Upper Carboniferous of the Czech Republic is just a wingless insect similar to a giant silverfish, and its position in the basal stem group of winged insects is only based on speculative scenarios and slightly broadened paranota. It basically is a fossil that roughly fits a hypothetical model (also see Haug et al. 2014, Ross 2017, 2022, Prokop et al. 2022), but not a transitional fossil in any meaningful way. It did not have anything like real mobile wings and not even anything that would be clearly identifiable as gliding or parachuting airfoils. There is no evidence or proof that it was an arboreal animal capable of gliding, and its large size rather points against this hypothesis. But including a fancy evolutionary story increased the unique selling point and impact of our paper, which I can freely admit now that I am no longer part of the Darwinian establishment and no longer under pressure from any museum PR departments to oversell results in the international competition for grants and reputation.
Devonian Proto-Wing Insects Debunked
What about alleged Devonian proto-winged insects you might have read about in text books. Don’t they prove a gradual development of wings from wingless insects prior to the Carboniferous period? No they definitely don’t do anything like that, as all known examples (Eopterum, Rhyniognatha, and Strudiella) for such alleged transitional fossils have been debunked:
Eopterum devonicum and Eopteridium striatum were described by the famous Russian paleoentomologist Rohdendorf (1961, 1970) as the oldest fossil evidence of winged insects from the Devonian of Russia. The fossils indeed resembled isolated insect wings with the characteristic wing venation. This finding made it into textbooks for decades, and was even featured in Willi Hennig’s (1969, 1981) groundbreaking work on Insect Phylogeny with detailed interpretation and naming of the wing venation. However, shortly later Rohdendorf (1972) himself already suspected that the two fossil may rather represent nothing but the isolated tail fans (uropods) of a fossil shrimp, which was strongly confirmed by the American crustaceologist Frederick Schram (1980). Bummer!
Rhyniognatha hirsti is a fragment of an arthropod head capsule from the Lower Devonian Rhynie chert in Scotland, which is about 412 million years old. The common claim that it represents the oldest insect fossil and possibly a winged insect is based on a study by Engel & Grimaldi (2004). Some experts tentatively followed their interpretation, such as Edgecombe & Legg (2013), who said that “Rhyniognatha is known from a mandible that is certainly a member of the insect clade Dicondylia (i.e. having an anterior mandibular articulation) and may even be a pterygote (Engel and Grimaldi 2004). Rhyniognatha (Fig. 15.6) extends the range of winged insects downwards from the Carboniferous.” Based on its characteristic morphology, I had always thought that Rhyniognatha rather looks like the head of a myriapod. Some colleagues from the University of Tübingen and the Natural History Museum in Stuttgart, with whom I had discussed the issue over the years fully agreed. Lo and behold, a more recent and much more thorough study by Haug & Haug (2017) suggested that Rhyniognatha was misinterpreted and indeed represents an early centipede, which was also accepted by Ross (2022).
Finally, Garrouste et al. (2012) described yet another supposed fossil evidence for a winged insect from the Late Devonian of Belgium, which they called Strudiella devonica. An accompanying comment to the original description celebrated the discovery because “a complete insect fossil from the Devonian period has long been sought” and “the finding of a candidate may improve our patchy understanding of when winged insects evolved” (Shear 2012). Otherwise, the identification of this fossil was immediately met with scepticism, because it lacked any trace of wings or even nymphal wing buds (Taylor 2012). Indeed, the fame of this fossil did not last long, because a year later a team of other distinguished scientists found that Strudiella is just a decomposing crustacean (Hörnschemeyer et al. 2013). They could hardly have been clearer when they said that “we consider it to be crucial to prevent this fossil from entering entomology textbooks as an early insect.” The original authors of course still disagreed (Garrouste et al. 2013), but most paleoentomologists no longer believe in this oldest winged insect and consider the identity of this fossil as problematic due to its poor preservation (Haug & Haug 2017).
After the debunking of Strudiella, evolutionary biologists were left empty handed with no fossil record at all of any Devonian precursors for winged insects that were postulated to exist by molecular clock studies and of course were expected by Darwinian reasoning based on the fully developed winged insects in the Lower Carboniferous (see below). Nevertheless, Darwinian scientists made grandiose claims like the following by Engel et al. (2013), which are not supported by any valid fossil evidence:
Palaeological studies have advanced significantly in the last twenty five years,particularly with a large number of reevaluations of taxa in a cladistic framework and by pushing back the timing of wing origins from the early Carboniferous into the earliest Devonian perhaps latest Silesian.
Clueless about wing origins.
The identification of putative proto-winged insects is also hampered by the more general problem that we do not even know how proto-wings should have looked like, because the question of insect wing origins is far from settled in the scientific community (see Grimaldi & Engel 2005, Engel et al. 2013, Ross 2017, 2022, Smith & Jockusch 2020, Akst 2022, Prokop et al. 2022). There exist very different theories for their origin without any consensus: Fossil evidence rather supports the older paranotal theory of an origin of insect wings from stiff outgrowths of the dorsal breastplates (paranota) of the exoskeleton, while evo-devo data rather support the newer exite theory (Kukalová-Peck 1997) of an origin from mobile leg appendages (exites). Actually, different lines of data equally support both theories, which are seemingly incompatible and mutually exclusive. This conundrum led to the suggestion that both theories might be true and insect wings originated as composite structures from a fusion of stiff thoracic outgrowths with mobile leg appendages. This dual origin hypothesis was also suggested in a paper co-authored by myself (Staniczek et al. 2011), but in this mainstream paper I could of course not mention the elephant in the room: such a view would make viable intermediate forms hardly conceivable, so that a saltational adaptive macro-mutation (hopeful monster) would be required, which would arguably imply intelligent design. Even though several recent studies (mainly by the research team of Tomoyasu and Clark-Hachtel at Miami University; e.g., Clark-Hachtel & Tomoyasu 2020) increasingly supported the dual origin hypothesis, there are also new studies that still support one of the single-origin scenarios, such as the recent Nature papers by Bruce & Patel (2020), who suggested “that insect wings and body walls evolved from ancient leg segments,” or by Ohde et al. (2022), who suggested “the wing origin from lateral tergum of a wingless ancestor.” Another recent study by Fisher et al. (2021) suggests that the evo-devo data “doesn’t favor either of those hypotheses about wings,” but rather, “what it says is we need other kinds of evidence” (Jockusch in Akst 2022). In other words, we are pretty much as clueless about the origin of insect wings as a century ago
The Oldest Fossil Record of Winged Insects
So, since all the alleged Devonian proto-winged insects have been debunked, what are the oldest unambiguous winged insects found in the fossil record? They were all found in Namurian sediments near the border between the Lower Carboniferous (Mississippian) and the Upper Carboniferous (Pennsylvanian), such as the rich fossil insect fauna from the Hagen-Vorhalle quarry in Germany, but many cannot be precisely dated enough to count them as oldest record (Brauckmann & Brauckmann 1992, Brauckmann et al. 1994, Prokop & Hörnschemeyer 2016). But there exist two exceptions, which happen to represent both major subgroups of winged insects (viz Palaeoptera and Neoptera).
One prominent contender is Delitzschala bitterfeldensis, which belongs to the palaeodictopterid family Spilapteridae and has even preserved the characteristic banded color pattern of the wings. It was discovered in the drilling core of a well borehole from the Bitterfeld region in eastern Germany (Brauckmann & Schneider 1996), which has been dated to a uppermost Lower Carboniferous age (Lower Namurian A/E2, Arnsbergian) of about 323 million years. Until recently this represented the oldest well-dated fossil of a winged insect (see Ross 2017) and has therefore been used as calibration point for phylogenetic trees (Wolfe et al. 2016).
More recently, an unnamed insect has been discovered in the slightly older (lowermost Namurian A/E1, Pendleian) sediments from the Upper Silesian Basin in the Czech Republic (Prokop et al. 2005), which are about 324 million years old. Based on its wing venation it could be attributed to the polyneopteran order Archaeorthoptera
The Oldest Fossil Record of Metamorphosis
Actually, the first holometabolous insects with complete metamorphosis are recorded from the same Pennsylvanian subperiod (about 314-307 million years ago) as many of the other very early winged insects (Nel et al. 2013). Molecular clock data even suggest that Holometabola are at least as ancient (about 328-318 mya) as the earliest fossil record of winged insects at all (Labandeira 2011), or place “the origin of Holometabola in the Carboniferous (355 Ma), a date significantly older than previous paleontological and morphological phylogenetic reconstructions” (Wiegmann et al. 2009a, 2009b, Misof et al. 2014). My dear colleague and frequent co-author André Nel (2019) recently commented that “the late Carboniferous was also the time of the oldest known holometabolous insects, with complete metamorphosis (wasps, beetles, scorpionflies).” Indeed, as already listed above, fossils from larval and adult holometabolous insects of different orders have been found in late Carboniferous layers (see Kukalová-Peck 1997, Nel et al. 2007, 2013, Béthoux 2009, Kirejtshuk & Nel 2013, Kirejtshuk et al. 2014, Haug et al. 2015). The mentioned holometabolan groups all have a complete metamorphosis with a pupal stage, where the caterpillar-like body plan of the larval stage is dissolved into a kind of cell tissue soup and rearranged into the very different adult body plan of the winged imago. It is hardly possible to explain an evolutionary origin of this marvellous metamorphosis at all, as the only suggested hypothesis, the so-called pronymph-hypothesis by Truman & Riddiford (1999), has to make the extremely implausible assumption that the main feeding stage (caterpillar) originated from a non-feeding late embryonal stage (pronymph) (see Bechly 2023b). Apart from that, it is certainly unexpected to find this sophisticated ontogenetic process already with early flying insects rather than after hundreds of millions of years of gradual evolution
Clocks versus Rocks
Just like in most other groups of organisms we find a great mismatch between the estimated ages by molecular clock studies and the earliest fossil record, even though Darwinism would predict that these two different lines of evidence should converge to the same true history of life. Molecular clock studies dated the origin of winged insects at about 440-370 million years ago, but the oldest fossil record is just about 324 million years ago, which implies a ghost lineage of a whopping 116-46 million years. (Gaunt & Miles 2002, Regier et al. 2004, Rehm et al. 2011, Rota-Stabelli et al. 2013, Thomas et al. 2013, Wheat & Wahlberg 2013, Misof et al. 2014, Rainford et al. 2014, Tong et al. 2015, Wang et al. 2016, Johnson et al. 2018, Montagna et al. 2019, Schachat et al. 2023).
New Study Vindicates the Carboniferous Insect Explosion
Last year a new study (Schachat et al. 2023), which reviewed the fossil and molecular evidence for the age of winged insects, fully vindicated the explosive origin of winged insects in the Carboniferous. In their abstract the authors confirmed the stark conflict between molecular clock datings and the fossil record, which requires extensive ghost lineages of unrecorded history. They were not at all convinced by any previous explanations for this conundrum and concluded:
Here, we examine the plausibility of such a gap in the fossil record, and possible explanations for it, … We do not find support for the mechanisms previously suggested to account for such an extended gap in the pterygote fossil record, including sampling bias, preservation bias, and body size.
Instead the authors suggested that the conflict between molecular clock and fossil record “is probably an analytical artifact of taxon sampling and choice of fossil calibration points, possibly compounded by heterogeneity in rates of sequence evolution or speciation, including radiations or ‘bursts’ during their early history [my emphasis].” Bursts in their early history is exactly what is described by me with the term Carboniferous Insect Explosion. I also agree that molecular clock datings are mostly rubbish, but this of course resonates better with intelligent design theory than Darwinian evolution, which would predict molecular clock studies to provide more accurate estimates on a regular basis.
The study also emphasized that different groups of insects appear in the fossil record roughly in the correct order as predicted by the sequence of branchings in phylogenetic reconstructions. Such cases of good stratigraphic fit indeed require an adequate explanation, which is arguably provided by common descent with modification. But the authors immediately qualified this result:
Obviously the fossil record is not sufficiently complete to expect that it recapitulates phylogeny with fine-tuned precision or accuracy, beyond the very broad-brush sequence of major taxa that are well represented as fossils; younger taxonomic units are expected to be less well represented as fossils, much less captured sequentially in the fossil record.
This suggests that the evidence for common descent from good stratigraphic fit may not be as strong as it is sometimes claimed.
Anyway, the abrupt appearance of winged insects with great diversity and disparity in the Carboniferous period, which we have called the Carboniferous Insect Explosion, is a phenomenon that is highly unexpected under Darwinian assumptions, but well be accommodated within an intelligent design paradigm. It represents just one of the many discontinuities in the history of life that strongly contradict the predictions from a neo-Darwinian theory of evolution. The same pattern is found in almost all groups of organisms, in all geographical regions, and in all periods of Earth’s history. This is clearly a signal in the data and not just noise. It is a signal that tells about a saltational history of life, with a series of bursts of biological creativity that can only be explained with the goal-directed infusion of new information from outside the system.
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