The Origin of Hexapods

Insects have been described as the most evolutionarily successful group of animals in the modern world, and with good reason. Something like two-thirds of the currently known animal species are insects, and they are near-ubiquitous in the terrestrial and freshwater environments (for whatever reasons, they've never made that much of a go of it marine-wise). Nevertheless, the questions of how and when insects first came to be remains very much an open one.

The long-necked fungus beetle Diatelium wallacei, one of the countless weird oddballs in the insect world. Copyright Artour Anker.

Insects are usually recognised as including three main subgroups: the winged insects, silverfish and bristletails. They are readily united into a group known as the hexapods with a few less speciose assemblages: the springtails, the proturans and the diplurans. All living hexapods have the body divided into a head, thorax and abdomen, with three pairs of walking legs on the thorax and none on the abdomen. Though monophyly of the hexapods has been questioned in the past (which is why the springtails and the like are usually excluded from our concept of 'insect' these days despite having been included previously), the majority view is now firmly in favour of regarding them as a single, coherent lineage. How hexapods are related to other arthropods has been more vigorously debated. Earlier authors commonly associated them with the myriapods, the lineage including centipedes and millipedes. In more recent years, an increasing number of studies have instead associated insects with crustaceans. This realignment has primarily been pushed by molecular studies but there are also a number of interesting morphological features such as eye and brain structure that are more crustacean- than myriapod-like in insects. Indeed, it seems not unlikely that insects are not merely related to but are nested within crustaceans: for instance, a few recent studies have supported a relationship between hexapods and a rare group of crustaceans known as remipedes (Schwentner et al. 2017). The features previously seen as shared between insects and myriapods, such as tracheae and uniramous (unbranched) limbs, are then held to probably be convergent adaptations to a terrestrial lifestyle.

Whatever its relationships, it seems most likely that the immediate ancestor of the living hexapods was indeed terrestrial. Of the six basal hexapod lineages referred to above, five (all except winged insects) are almost exclusively terrestrial and were probably ancestrally so. The winged insects include a number of basal subgroups (such as mayflies and dragonflies) that are aquatic for at least the early part of their life cycle, but a terrestrial origin for winged insects as a whole remains credible.

Head of Rhyniella praecursor, from Dunlop & Garwood (2017).

From the perspective of the fossil record, the evidence related to hexapod origins is incredibly slight. The earliest fossil species that have been directly proposed as hexapod relatives are known from the Early Devonian and less than half a dozen such species have been mooted as such in recent years. The only named Devonian fossil whose status as a hexapod seems unimpeachable is Rhyniella praecursor, a springtail from the Rhynie chert of Scotland (Dunlop & Garwood 2017). The same deposit provided Rhyniognatha hirsti, a fragmentary fossil comprising a pair of mandibles and surrounding parts of the head capsule. Rhyniognatha has long been thought to be an insect, possibly even an early member of the winged insect lineage, but Haug & Haug (2017) recently argued that it could just as easily be the head of a centipede (a group already known from other fossils in the Rhynie chert).

Rhyniognatha hirsti, from the University of Aberdeen. Scale bar = 200 µm; m = mandible.

The Windyfield chert, a deposit of similar age and location to the Rhynie chert, has provided Leverhulmia mariae, originally described as a myriapod but reinterpreted as a hexapod relative by Fayers & Trewin (2005). Leverhulmia is a difficult beast to know what and how much to make of it. The original specimen is, speaking charitably, a bit of a mess: a flattened smear looking a bit like a sausage burst open after cooking for too long on the pan. The front and back ends of the animal both appear to be missing and the only features really distinguishable are a series of small jointed legs. Other specimens associated with this species by Fayers & Trewin (2005) are simply more legs detached from their original body. These legs, though, do preserve a reasonable amount of detail, including the presence of paired lateral claws at the ends of the tarsi like those of most insects (Leverhulmia also possesses a smaller median claw between the lateral claws, a feature not found in winged insects but present in silverfish and bristletails). In contrast, the legs of myriapods (as well as those of springtails and proturans) end in a single terminal claw.

Holotype specimen of Leverhulmia mariae, from Dunlop & Garwood (2017); the size of the scale bar was not specified but the entire specimen is about 12 mm long.

The overall appearance of Leverhulmia's legs might therefore be seen a suggestive of a relationship specifically to insects and not just to hexapods in general, but their number provides something of a barrier to accepting Leverhulmia as a bona fide insect. The train-wreck nature of Leverhulmia's preservation means we can't state confidently how many legs it had but there were at least five pairs: a couple more than the hexapods' standard-issue three. A number of structures on the abdomens of some living hexapods are potentially derived from modified legs, such as the springing furca of springtails and the ventral styli in hexapods other than springtails and winged insects, so some parallelism in appendage reduction is not out of the question. Nevertheless, unjointed styli are one thing; fully-jointed, functional walking legs are another. Supposed early members of the bristletail and silverfish lineages with jointed abdominal legs have been described from the Carboniferous by Kukalová-Peck (1987) but (as I've noted before) many of the more outlandish reconstructions of early insects by Kukalová-Peck have failed to stand up to subsequent scrutiny.

Similar interpretative difficulties surround Strudiella devonica, described as an early relative of the winged insects from the Late Devonian of Belgium. Though I was not unfavourable to this specimen when it was first described, Hörnschemeyer et al. (2013) would later argue against recognising it as an insect. The latter authors professed to be simply unable to discern many of the features cited by its original describers as evidence of insect affinity, and saw Strudiella as closer to a Rorschach blot than a dragonfly. Strudiella's status was defended by its original authors (Garrouste et al. 2013) but a number of subsequent authors seem to have taken Hörnschemeyer et al.'s caution to heart.

Close-up of the head of Strudiella devonica from Hörnschemeyer et al. (2013); the asterisk marks the base of a structure originally interpreted as an antenna.

The final candidate for stem-hexapod status worthy of consideration here is Wingertshellicus backesi from the Lower Devonian Hunsrück Slate of Germany. This marine fossil was interpreted as a stem-hexapod under the name Devonohexapodus bocksbergensis, with a thorax bearing three pairs of legs and an elongate abdomen with uniramous appendages. However, it was reinterpreted by Kühl & Rust (2009) who synonymised Devonohexapodus with the previously described Wingertshellicus, regarded the previously described 'thoracic legs' as appendages of the head, and did not accept the presence of differentiated thorax and abdomen. The appendages of the trunk (previously seen as the abdomen) were biramous rather than uniramous with a small endopod and a large flap-like exopod adapted for swimming, and the end of the body bore a pair of fluke-like appendages (comparable to the tail of a crayfish). Wingertshellicus thus lacked any resemblance to a hexapod, and Kühl & Rust doubted that it even belonged to the crown group of arthropods.

Laterally preserved specimen of Wingertshellicus backesi, from Kühl & Rust (2009); scale bar = 10 mm.

An attempt to estimate the age of divergence of hexapods from other arthropods using a molecular clock analysis by Schwentner et al. (2017) suggested that hexapods and remipedes went their separate ways in the late Cambrian or early Ordovician. This is up to 100 million years earlier than the fossils described above but we should be careful how much to read into this discrepancy. If most of the features associated with hexapods are related to adoption of a terrestrial lifestyle, then it might be difficult to recognise any early marine relatives if found. Conversely, while it is uncertain how much if any terrestrial vegetation was present prior to the Devonian, the only potential cover would have been low lichens, non-vascular plants or micro-algae. If stem-hexapods emerged onto land during this time, the environment would not be conducive to their preservation in the fossil record. Finally, not only are hexapods other than winged insects not found in the fossil record before the Devonian, they are barely found after it: after Rhyniella, none are known until the appearance of amber-producing trees during the Cretaceous. So if we can't find any sign of them for some 300 milion years that we know that they are around, then we obviously can't say too much about not finding them over the previous hundred million years. The stem-hexapods may have been around in this time but they remain in hiding.

REFERENCES

Dunlop, J. A., & R. J. Garwood. 2017. Terrestrial invertebrates in the Rhynie chert ecosystem. Philosophical Transactions of the Royal Society of London Series B—Biological Sciences 373: 20160493.

Fayers, S. R., & N. H. Trewin. 2005. A hexapod from the Early Devonian Windyfield Chert, Rhynie, Scotland. Palaeontology 48 (5): 1117-1130.

Garrouste, R., G. Clément, P. Nel, M. S. Engel, P. Grandcolas, C. D'Haese, L. Lagebro, J. Denayer, P. Gueriau, P. Lafaite, S. Olive, C. Prestianni & A. Nel. 2013. Is Strudiella a Devonian insect? Garrouste et al. reply. Nature 494: E4–E5.

Haug, C., & J. T. Haug. 2017. The presumed oldest flying insect: more likely a myriapod? PeerJ 5: e3402.

Hörnschemeyer, T., J. T. Haug, O. Bethoux, R. G. Beutel, S. Charbonnier, T. A. Hegna, M. Koch, J. Rust, S. Wedmann, S. Bradler & R. Willmann. 2013. Is Strudiella a Devonian insect? Nature 494: E3–E4.

Kühl, G., & J. Rust. 2009. Devonohexapodus bocksbergensis is a synonym of Wingertshellicus backesi (Euarthropoda)—no evidence for marine hexapods living in the Devonian Hunsrück Sea. Organisms, Diversity & Evolution 9: 215–231.

Schwentner, M., D. J. Combosch, J. P. Nelson & G. Giribet. 2017. A phylogenomic solution to the origin of insects by resolving crustacean-hexapod relationships. Current Biology 27: 1818–1824.