The first land animals to appear in the fossil record are not four-footed vertebrates but millipedes. Old Red Sandstone deposits in Aberdeenshire have revealed that millipedes date back to at least the mid Silurian. ‘The first air-breathing animal was Scottish’ ran the jubilant headline of Scotland’s Sunday Herald when the find was announced. In fact the record-holder was English, since Ordovician trackways of what seem to have been millipedes have been found in the Lake District even further back. Despite assertions to the contrary (by David Attenborough among others), there is no evidence that insects, millipedes, centipedes and spiders emerged from the sea. Indeed there are no fossils at all to link them to earlier animals of a different identity. As the discoverers of the Scottish animal noted (Wilson & Anderson 2004), ‘The oldest known millipedes were fully terrestrial.’ They had the spiracles and tracheal system of air-breathers. Moreover, the co-existence of an entirely different order of millipede of mid-Silurian date shows that amazing land-dwellers already had a considerable evolutionary history behind them – hence the appearance of trackways in the Ordovician, only a little after the explosive arrival of marine animals.
Invertebrates can be classified into around 30 fundamental body plans, termed phyla. Of these groups, only 3 are known to have made it onto land: annelids, represented today by (for example) earthworms, onychophorans, represented by velvet worms, and molluscs, represented by slugs and snails. Arthropods – a mixed bag – may be a fourth if it turns out that scorpions emerged from the sea.
Other arthropods, including insects and millipedes, show no indication of having had marine equivalents, and appeared on the scene within a remarkably brief span of time. Centipedes are known from the late Silurian, as are the extinct spider-like animals called trigonotarbids and an extinct myriapod called Eoarthropleura. The oldest true spider dates to the early Devonian. So does the oldest harvestman, another spider-like animal. In the paper reporting this find the harvestman was said to suggest ‘an extraordinary degree of morphological stasis … with the Devonian forms differing little in gross morphology from their modern counterparts’. In other words, their fossil record shows hardly any evolution.
The catalogue from the Devonian is a mix of the familiar and the unfamiliar. Other terrestrial invertebrates that appeared then include mites, springtails, bristletails, pseudoscorpions (tiny, still extant creatures that look like scorpions, except that they have no tail) and a second order of arthropleurid known as Microdecemplex. Arthropleurids looked rather like millipedes, but differed in too many respects to be put in the same taxonomic class. Eoarthropleura and Microdecemplex became extinct around the end of the Devonian. A third order, Arthropleura itself, appeared in the Carboniferous and was a much larger animal than the others, with some examples attaining a length of more than 2 metres. It fed on rotten tree trunks and other such litter, becoming extinct in the Permian.
All these distinct kinds were joined in the Carboniferous by a host of other land-dwelling invertebrates, most of them with wings (another mysterious innovation): mayflies, dragonflies, cockroaches, crickets, as well as numerous extinct groups. “The two very first winged insects that we have in the fossil record, they’re about as different from each other as you could imagine,” admits entomologist Sandra Schachat (Sci. Am. 318, 18 (2018)). Around 17 orders of insects are known from the period, most of which seem to have evolved ex nihilo. After their first appearance, they increased in number of species spectacularly.
What we witness is evolution on an amazing scale. Only it is not Darwinian evolution. However many new species arose, they retained the essential identity of their order. The latest cockroaches were still cockroaches, the latest mayflies still mayflies.
There were, eventually, many new species. Consider the scorpions, which like the millipedes first appeared in the mid Silurian. Numbering today around 1,100 species, the group is not especially diverse, and was probably more diverse in the past. Nonetheless, if each species, on a conservative estimate, lasted on average 3 million years in geological time, the total number of scorpion species would be in the hundreds of thousands.
That is problematic. According to Darwin, the difference that distinguished each new species had to have arisen by chance, as the advantage conferred by the difference enabled the population to leave more offspring and outcompete other species. But the sheer number of species strains the idea to breaking point. As often as not, animals appear to have increased in diversity because they were colonising new territory and niches – avoiding competitors rather than competing with them. While it is true that they needed to adapt in such circumstances and adaptation involves differentiation, they were spreading abroad before their habitats became overcrowded. Until they had their adaptations, their new surroundings put them at a disadvantage, not an advantage. Had they been obliged to wait on ‘chance’ to equip them with what they needed, they would have been wiped out. Their evolution must have been foreordained. Dispersal and adaptation went hand in hand.
Millipedes, centipedes, spiders and insects did not originate from marine precursors. Nor did plants. As we search for an explanation, perhaps there are clues to be found in observing how invertebrates recolonise empty territory after volcanic eruptions, such as the island of Surtsey or Mt St Helens. Typically the first animals to invade are insects, mites and spiders, and they do so by falling out of the sky, swept up by winds and borne in the air over hundreds of miles. Similarly, wind-transport may have been the way in which invertebrates reached new land after the end-Hadean cataclysm. Most of them were tiny, less than 2 cm in length. They were transported over the world involuntarily, like plant spores. Animals that were heavier and reproduced less prolifically arrived later (how late, depending on the distance travelled) and mostly on foot.
Water would have provided another means of transport. The cuticles of many springtails are water-repellant, and experiments have shown that even in agitated seawater springtails can survive for weeks. While their mode of transport is not known, within ten years of Surtsey Island’s formation no fewer than six species of springtail had reached its shores.
The first animals were extremely sparse, becoming more common as time goes on. This is anomalous in a scenario where innovations became fixed in populations because more of the offspring survived. Over tens of thousands of years, a mere instant in geological time, invertebrates taking advantage of the opportunities provided by plants might be expected to have overrun the earth, and ought to have been as abundant at the beginning of the multimillion-year period in which they originated as at any other time. But the actual interval between their first appearance and what might be considered normal population levels is typically measured in tens, even hundreds, of millions of years. The pattern fits neither the theory of evolution nor its associated timescales. It shows that populations were initially few and far between, but gradually increased. Where the first populations came from no one can say, since going back in time the trail peters out.
That they were preceded by a substantial history is clear. However sparse, their fossils rarely occur in contexts which suggest they were the very first generation of pioneers – isolated, starved of sustenance and perishing where they dropped. Invertebrates tend to occur in association and close to plant material, as part of assemblages constituting the remains of some sort of ecosystem. The assemblages in the Ludford Lane Bonebed or the Rhynie Chert (both, as it happens, in the UK) are spectacular. Evidently the plants were there before the animals, and the animals were either living off the plants or off each other: the insects using their mandibles to nibble on the spores, the spiders preying on the insects. The simultaneous appearance of diverse groups of organisms, unrelated ancestrally but related ecologically, is of the essence of recolonisation.
In the next article we look at the story of how vertebrates conquered the land. Although invertebrates fail to substantiate the Darwinian story – even aquatic scorpions were still scorpions after the transition – fish might present a more convincing case. The claim is that at least one lineage evolved limbs, air-breathing apparatus and a great array of other apparently miraculous changes, until it abandoned the water altogether and attained the state of reptile. Anything is possible in the natural world. A tadpole can sprout legs and evolve into a frog in a single generation. Did fish manage to do the same in the course of twenty million years?