The most primitive living insects are thought to be bristletails (see below), also called jumping bristletails, which are placed in the Order Archaeognatha (Class Insecta) (Grimaldi & Engel, 2012). These primitive little wingless insects – not to be confused with silverfish (Zygentoma), which are also very old – have persisted since at least the mid-Devonian epoch (398–385 million years ago [Myr]). The lack of wings has not impeded the lengthy existence of these insects or hindered their diversification into a wide range of habitats, worldwide (Gaju-Ricart et al., 2015). However, the evolution of wings was a hugely significant development, which supercharged the diversification of insects, such that there are now more described species of winged insects (Pterygota) than all other multicellular life (Grimaldi and Engel, 2005).
N.B. The oldest, definitively winged insects are from the Early Carboniferous period (circa 324 Myr) (Prokop et al., 2005). Arthropods (and vertebrates as well) went through two main periods of diversification, firstly in between the Silurian and the Late Devonian period (425–385 million years (Myr) ago); and secondly, during the Late Carboniferous period (after 345 Myr ago) (Garrouste et al., 2012).
The integument of both bristletails and silverfish are covered with scales that sometimes form colourful patterns (below). It’s interesting to note that trees first appeared about the same time as these early insects – the ancestors of the modern day versions shown here – began to crawl onto the land, in the mid-Devonian (398–385 Myr).
According to Engel (2015), ‘the apterous orders of bristletails (Archaeognatha) and silverfish (Zygentoma) give us our closest concept of what the original insect might have resembled.’ Meaning they looked a bit like this! See below.
The early trees which appeared in the mid-Devonian were not trees as we know them – i.e. angiosperms and gymnosperms – but lycophytes and cladoxylopsids (below), which are related to modern ferns and horsetails. It is somewhat surreal, to think of the tiny primitive arthropods running around on the ground beneath these strange, hollow trees, which grew up to eight metres tall.
Going back further from the appearance of insects in the Devonian, the first arthropods to emerge from the sea and occupy terrestrial habitats – probably in the Late Silurian – were myriapods (centipedes and millipedes) and arachnids (Gueriau et al., 2020). The oldest unequivocal myriapod fossil is of the millipede, Pneumodesmus newmani (below), from the late Silurian (428 million years ago). Centipedes and millipeds deserve respect for being so old!
The earliest Arthropods, such as trilobites, appeared even earlier, during the Cambrian period, but were still around during the Devonian (see below) when terrestrial insects first appeared. However, there are many uncertainties concerning the early origins of the class Insecta, mainly because of the dearth of well preserved early fossils, particularly during the Early–Middle Devonian (411.5–391 Myr ago).
Hexapods (Hexapoda) – i.e. arthropods with six legs – have been around for a very long time: probably originating in the Early Ordovician, sometime between 509 to 452 Myr, according to phylogenomic analyses of nucleotide and amino acid sequences (Misof et al., 2014), although it is important to emphasise that there is no fossil evidence of terrestrial hexapods from this period.
‘Insects comprise the more diverse of two classes united together as the arthropod subphylum Hexapoda, the other being the Entognatha, consisting of the orders Diplura (below), Protura, and Collembola (springtails)’ (Engel, 2015).
Fossil springtails (Collembola) have been found in the lower Devonian, Rhynie chert, in Rhynie, Scotland; dating from about 396–407 million years ago (below). Whole communities of plants, algae, fungi, arthropods (e.g. centipedes, harvestmen) and other invertebrates were preserved in this rock by the action of hydrothermal hot springs depositing silica. These cherts provide superb in situ preservation of an entire ecosystem – see here and here – from the Lower Devonian, including both freshwater and terrestrial arthropods (Trewin and Kerp, 2017).
A number of hexapod species have been found in the cherts at Rhynie. The springtail, Rhyniella praecursor – see here and below – from the Lower Devonian Rhynie chert (c. 410 million years ago) is considered to be the oldest hexapod, and possibly the oldest true insect (Ectognatha) (Engel and Grimaldi, 2004).
The other forms found in the cherts at Rhynie, include the collembolan, Rhyniella praecursor, and the pterygote insect Rhyniognatha hirsti, discovered in 1919. Another possible hexapod, somewhat resembling a silverfish and possibly the earliest known wingless insect, called Leverhulmia mariae, was found in the nearby, Windyfield chert, also from the Early Devonian. This species was originally described as a myriapod but subsequently reinterpreted as a hexapod by Fayers & Trewin (2005). The Windyfield chert, is located only some 700 m away from the Rhynie chert and is of a similar age, containing fossils of a range of other arthropods, including brine shrimps, centipedes, myriapods and others.
However, all of these scarce, putative fossil insects from the Devonian are considered to be ‘problematic and controversial’ due to their incomplete preservation and because of the difficulties of interpreting the fossilised fragments (Haug and Haug, 2017). So much so, that Carolin and Joachim Haug from the Ludwig-Maximilians Universität München, in Germany, reinterpreted what was originally thought to be the oldest flying insect, Rhyniogatha hirsti, as an early centipede! Shown below in a magnificent illustration.
Another early insect from Late Devonian sediments in Belgium, named Strudiella devonica, was probably a terrestrial species (see below). The discovery of Strudiella devonica, in association with numerous other arthropods – Crustacea and Chelicerata – was said to narrow the 45-Myr hexapod gap in the fossil record (see below), and demonstrate a first Devonian phase of diversification for the Hexapoda (Garrouste et al., 2012).
This transition from the water to the land – often called terrestrialisation – involved a number of novel adaptations, including: osmoregulation (to avoid dehydration), respiration and reproduction in the air rather than in water, locomotion without the air of buoyancy, and exposure to ultraviolet radiation (Dunlop et al., 2013). These adaptations may have evolved under the selection pressures of severe drought during the Devonian period. The drying up of freshwater habitats may have forced hexapods – as well as tetrapods – onto the land (Glenner et al., 2006). These early terrestrial hexapods probably fed on the sporangia of algae and fungi, or scavenged on organic matter.
The hexapod gap
As described above, fossils of so-called stem group hexapods are rather rare, so there is relatively little evidence to connect hexapods to the other major arthropod subphyla, such as Crustacea, Myriapoda and Chelicerata (Engel, 2015). This period in the fossil record has been called the hexapod gap (see below), and encompasses the entirety of the Late Devonian (383–359 Ma) and the Mississippian sub-period (359–323 Ma) of the Carboniferous.
For much of the past 325 million years or so, there is a fairly extensive insect fossil record – with at least 1,263 families represented by one or more specimens – even though only a small fraction of these fossil insects have been formally described (Labandeira and Sepkoski, 1993; Clapham et al., 2016). Nevertheless, a full understanding of the evolution of insects is still lacking due to the absence of direct fossil evidence from the early period of hexapod evolution (Wang et al., 2016). In addition, our knowledge of the evolution of insects is based on a total of about 25,000 species of fossil insects that have been examined and described, out of a total of what may have been more than a billion insect species, over their c. 410+ Myr, or so, history (Willmann, 2004). That’s a tiny percentage of the total picture. Like staring through a dark canvass, with just a few chinks of light illustrating the picture unfolding behind the curtain.
It’s nice to think that fossils will continue to be found – they must be there in the rocks waiting to be unearthed! – which will undoubtedly shed more light on the early emergence of insects.
Insects took off when they evolved wings
Bradley, T. J., Briscoe, A. D., Brady, S. G., Contreras, H. L., Danforth, B. N., Dudley, R., … & Yanoviak, S. P. (2009). Episodes in insect evolution. Integrative and Comparative Biology, 49(5), 590-606.
Clapham, M. E., Karr, J. A., Nicholson, D. B., Ross, A. J., & Mayhew, P. J. (2016). Ancient origin of high taxonomic richness among insects. Proceedings of the Royal Society B: Biological Sciences, 283(1824), 20152476.
Dunlop JA, Scholtz G, & Selden PA. 2013. Water-to-land transitions. In: Arthropod biology and evolution: molecules, development, morphology (eds Minelli A, Boxshall G, Fusco G), pp. 417-439. Heidelberg, Germany: Springer.
Engel, M. S. (2015). Insect evolution. Current Biology, 25(19), R868-R872.
Engel, M. S., & Grimaldi, D. A. (2004). New light shed on the oldest insect. Nature, 427(6975), 627-630.
Fayers, S. R., & Trewin, N. H. (2005). A hexapod from the early Devonian Windyfield chert, Rhynie, Scotland. Palaeontology, 48(5), 1117-1130.
Gaju-Ricart, M., Baltanás, R. M., & de Roca, C. B. (2015). Forward without wings: current progress and future perspectives in the study of Microcoryphia and Zygentoma. Soil Organisms, 87(3), 183-195.
Garrouste, R., Clément, G., Nel, P., Engel, M. S., Grandcolas, P., D’Haese, C., … & Nel, A. (2012). A complete insect from the Late Devonian period. Nature, 488(7409), 82-85.
Glenner, H., Thomsen, P. F., Hebsgaard, M. B., Sørensen, M. V., & Willerslev, E. (2006). The origin of insects. Science, 314(5807), 1883-1884.
Haug, C., & Haug, J. T. (2017). The presumed oldest flying insect: more likely a myriapod?. PeerJ, 5, e3402.
Labandeira, C. C., Beall, B. S., & Hueber, F. M. (1988). Early insect diversification: evidence from a Lower Devonian bristletail from Québec. Science, 242(4880), 913-916.
Labandeira, C. C., & Sepkoski Jr, J. J. (1993). Insect diversity in the fossil record. Science, 261(5119), 310-315.
Misof, B., Liu, S., Meusemann, K., Peters, R. S., Donath, A., Mayer, C., … & Zhou, X. (2014). Phylogenomics resolves the timing and pattern of insect evolution. Science, 346(6210), 763-767.
Nel, A., Roques, P., Nel, P., Prokin, A. A., Bourgoin, T., Prokop, J., … & Kirejtshuk, A. G. (2013). The earliest known holometabolous insects. Nature, 503(7475), 257-261.
Nicholson, D. B., Ross, A. J., & Mayhew, P. J. (2014). Fossil evidence for key innovations in the evolution of insect diversity. Proceedings of the Royal Society B: Biological Sciences, 281(1793), 20141823.
Prokop, J., Nel, A., & Hoch, I. (2005). Discovery of the oldest known Pterygota in the lower Carboniferous of the Upper Silesian Basin in the Czech Republic (Insecta: Archaeorthoptera). Geobios, 38(3), 383-387.
Shear, W. A. (2012). An insect to fill the gap. Nature, 488(7409), 34-35.
Strullu-Derrien, C., Kenrick, P., & Knoll, A. H. (2019). The Rhynie chert. Current Biology, 29(23), R1218-R1223.
Trewin, N. H., & Kerp, H. (2017). The Rhynie and Windyfield cherts, Early Devonian, Rhynie, Scotland. In Terrestrial conservation Lagerstätten. Windows into the evolution of life on land (pp. 1-38). Dunedin Academic Press Edinburgh, UK.
Tihelka, E., Howard, R. J., Cai, C., & Lozano-Fernandez, J. (2022). Was There a Cambrian Explosion on Land? The Case of Arthropod Terrestrialization. Biology, 11(10), 1516.
Willmann, R. (2004). Phylogenetic relationships and evolution of insects. In: Assembling the tree of life, pp. 330-344. Oxford University Press.
Next time I meet a centipede or millipede I’ll certainly pay them due deference. Thank you for taking us on a fascinating journey. 😊