The Invasion of the Continents

Due to the inherent time constraints of having to compress what is usually a semester's worth of knowledge into 4.5 hours, we will now move away from the oceans permanently and look at the rest of the history of life on Earth from only a terrestrial perspective.

To do that, we have to first examine what challenges awaited those few organisms that made the transition to land. Then we will see how they evolved and radiated further, and ending with the most severe mass extinction in the history of life on Earth.

The earliest terrestrial life is preserved in the Gunflint Chert, 2.1 Ga, Canada, and consisted of cyanobacterial colonies. Later, fungi also made the jump (lower pictures). These groups made an important contribution by beginning to break down the rock and starting to form the first soils, undoubtably a very important foundation for the pioneering first plants.

Upper picture source: Schopf, J. W., Kudryavtsev, A. B., Agresti, D. G., Wdowiak, T. J. & Czaja, A. D. 2002. Laser-Raman imagery of Earth's earliest fossils. Nature 416, 73-76. DOI: 10.1038/416073a

Lower pictures source: Yuan, X., Xiao, S. & Taylor, T. N. 2005. Lichen-like symbiosis 600 million years ago. Science 308, 1017-1020. DOI: 10.1126/science.1111347

These land plants are derived from green algae (Chlorobionta). The truly terrestrial plants are the embryophytes.

The most basal embryophytes are the bryophytes, a group that includes mosses, liverworts and hornworts. They show several key adaptations to life on land. The first is the presence of leaves and stems.

Importantly, these structures are covered by a waterproof cuticle: one of the main challenges of moving from water to land is the need to conserve water.

Another adaptation to help with preventing water loss is stomata, holes in the leaves that control exchange gas exchange and water balance. These are not present in liverworts, though.

Another important adaptation is the development of spores. A side-effect of spores is that they are easily preserved. The earliest spores are shown above, from 470 Ma of Oman.

We can be fairly certain that these spores are liverwort spores because of their characteristic shape – these spores are the earliest direct evidence for land plants.

As for the earliest body fossil of a bryophyte, the Lower Devonian fossil Sporogonites is accepted by most authors to be a sporing liverwort that is flattened (reconstruction pictured).

Out of the embryophytes evolved the tracheophytes, the plants with tracheae.

The tracheophytes include all land plants besides the bryophytes, and the basal representatives include the horsetails (Equisetopsida), spikemosses (Lycophyta) and ferns (Filicopsida).

As the name suggests, tracheophytes have vascular bundles. These are the xylem for water transport and phloem for nutrient transport. Additionally, tracheophytes have cambium, which is a structural tissue that gives the plant rigidity, allowing it to grow taller and wider (a key prerequisite for wood).

The earliest tracheophytic plant is Cooksonia caledonica from the Silurian and surviving until the Early Devonian.

Cooksonia belonged to the Rhyniopsidae family; a concurrent trachaeophyte family was that of the zosterophyllids, whose representatives had numerous lateral sporangia instead of one (see top of the plants).

These early trachaeophytes were relatively short-lived, and they were soon replaced by spikemoss-like plants as the dominant vegetation.

Now that we have an idea whatt he vegetation was like, we can look at the animals that started populating it.

The most significant animal group that made the transition to land is the arthropods. They were also the first animals on land. Of the five arthropod subphyla that have existed, four have managed to conquer the land.

Crustacea have done it multiple times: above, a pillbug (Isopoda) is pictured; crabs are another example.

Insecta are now thought to be crustaceans, but for the sake of practicality and familiarity, I will treat them separately. They transitioned to land only once.

Chelicerata are the spiders, scorpions and their relatives. It is currently controversial whether they came on land once or multiple times.

Myriapoda are the millipedes and centipedes, and they came on land once.

The very first animals on land were the euthycarcinoids, an enigmatic group of arthropods whose systematic placement is still up in the air. In the past it was suggested that they are at the base between a myriapod-insect split, but nowadays, insects are considered to be crustaceans, so this placement is unlikely.

Regardless of what they are phylogenetically, they left numerous trackways on Cambrian beaches.

Body picture: Racheboeuf, P. R., Vannier, J., Schram, F. R., Chabard, D. & Sotty, D. 2008. The euthycarcinoid arthropods from Montceau-les-Mines, France: functional morphology and affinities. Earth and Environmental Science Transactions of the Royal Society of Edinburgh 99, 11-25. DOI: 10.1017/S1755691008006130

Tracks: MacNaughton, R. B., Cole, J. M., Dalrymple, R. W., Braddy, S. J., Briggs, D. E. J. & Lukie, T. D. 2002. First steps on land: Arthropod trackways in Cambrian-Ordovician eolian sandstone, southeastern Ontario, Canada. Geology 30, 391-394. DOI: 10.1130/0091-7613(2002)030<0391:FSOLAT>2.0.CO;2

As for the earliest animal body fossils, they belong to the myriapods, who have a terrestrial fossil record as early as the Silurian.

Pictures source: Wilson, H. M. & Anderson, L. I. 2004. Morphology and taxonomy of Paleozoic millipedes (Diplopoda: Chilognatha: Archipolypoda) from Scotland. Journal of Paleontology 78, 169-184. DOI: 10.1666/0022-3360(2004)078<0169:MATOPM>2.0.CO;2

Now we come to the most numerous and diverse of all terrestrial organisms, the hexapods, which includes the insects.

The earliest hexapod known is Rhyniella praecursor from the 408 Ma Rhynie Chert of Scotland - the same locality where Cooksonia (and numerous other very cool organisms) are preserved in high-detail 3D.

Rhyniella can confidently be assigned as a springtail (Collembola) due to it having a collophore, a pair of eversible vesicles at the tip of a ventral tube on the 1st abdominal segment, only found in collembolans.

The presence of Rhyniella hints that hexapods had already diversified.

Foolproof evidence of extensive diversification having already taken place is also available from the Rhynie Chert: this pair of mandibles termed Rhyniognatha hirsti. They have a dicondyle structure, which is typical of the derived hexapods known as insects.

In fact, it is also possible that these are the mandibles of a flying insect – meaning wings had already evolved and the air already conquered.

Redescription of Rhyniognatha : Engel, M. S. & Grimaldi, D. A. 2004. New light shed on the oldest insect. Nature 427, 627-630. DOI: 10.1038/nature022291

Another early insect is Dasyleptus from the Permian of Russia. While it is an insect, it is not a flying insect, but a silverfish relative.

Diagram source: Grimaldi, D. 2010. 400 million years on six legs: on the origin and early evolution of Hexapoda. Arthropod Structure & Development 39, 191-203. DOI: 10.1016/j.asd.2009.10.008

Picture source: Grimaldi, D. & Engel, M. 2005. The Evolution of the Insects. Cambridge University Press.

The diagram shows the available fossil record, with thick lines indicating where fossils are present and thin lines representing ghost lineages – the organisms must have been alive, but we have no fossil record of them.

When there is such a large gap in the fossil record of a taxon, we refer to it as a Romer's gap.

Finally, we come to the chelicerates. Really, they have only a single key adaptation to life on land: their book lungs, which allow them to breathe outside of water.

As I said before, it is controversial whether the chelicerates came on land once or multiple times. The issue centers on the one hand around homology of the book lungs: if looking at recent lineages, we find that scorpion and spider book lungs are homologous, i.e. that they have a single origin from a last common ancestor, who must have been terrestrial.

However, the fossil record shows marine scorpions after the earliest land spiders (e.g. in the Hunsrück Slates). This could mean two things: either these scorpions secondarily went back to a marine lifestyle, or the scorpions (who have no early terrestrial fossil record) came on land independently of the spiders.

Time, but especially research, will tell which hypothesis is more likely. But this is a neat example for how palaeontology can provide crucial counterevidence to hypotheses based on modern taxa only. Ignoring the fossil record should be considered very unwise.

With the arthropods on land, the only remaining animal group is the vertebrates. All terrestrial vertebrates are derived from lobefinned fish, with the pectoral fins gradually being modified into walking limbs.

We have several transitional fossils and trackways that show this transition from marine to terrestrial life, the most significant one being Tiktaalik. I recommend visiting the the Your Inner Fish website advertised above (and buying the book!), as well as the Tiktaalik website at http://tiktaalik.uchicago.edu/

Two other famous transitional forms, known especially from childhood (at least for anyone who was in their teens and older in the 2000s) are Ichthyostega and Acanthostega, both pictured above.

Besides the changes in the limb morphology, a rib cage was also developed in order to provide more support. Basically, the challenge for life on land for a vertebrate is getting the skeleton to get used to the lack of buoyancy.

The above summarises very shortly some of the temporal milestones.

Now that we have animals and plants on land, let's see how the vegetation developed further.

The next period of time is the Carboniferous and, as the name suggests, this is when great coal forests developed, with trachaeophytes radiating.

A key component of this radiation was competition – and plants classically compete for sunlight, i.e. they generally push each other to grow taller. And that they did, with 15 m high ferns, 20 m high horsetails and 35 m high lycopsids. While none of these groups can develop wood per se, their trunks had a wood-like texture and they could rightly be called "trees".

This is what a typical coal forest would have looked like – warm, humid and swampy. However, it is important to keep in mind that this was not so everywhere on the globe.

This type of biome was present in tropical areas, but further out were temperate forests. However, due to swampy areas having a much higher preservation potential (the mud pits are anoxic!), much more is known about them.

In the Carboniferous, we have the very sudden appearance of a high diversity of flying insects. In fact, many of the insect orders known today were already living in the Carboniferous forests, as well as many now-extinct orders.

This is apparently an explosive radiation, but it may be another case of a Romer's gap, as we don't really have any transitional fossils showing the stem-groups of these very diverse insect orders. Unlike the Cambrian Radiation, where the stem-group fossils are there, here we really are dealing with a gappy fossil record and only an apparent burst of diversity, not a real one – although this conclusion can be disputed as well!

In this diagram, the still-living orders that originated in the Carboniferous are: the mayflies (Ephemeroptera), dragon- and damselflies (Odonata), grasshoppers, crickets and their ilk (Orthoptera) ...

Diagrams source: Labandeira, C. C. & Eble, G. J. 2005. The fossil record of insect diversity and disparity. In: Anderson, J., Thackeray, F., van Wyk, B. & de Wit, M. (Eds.). Gondwana Alive: Biodiversity and the Evolving Biosphere. Witwatersrand University Press.

… roaches (Blattodea) and plant bugs (Hemiptera).

Of course, the Carboniferous is also famous for its giant arthropods, popularised by Starship Troopers (a movie as accurate as The Core).

A much better popularisation is the part of the BBC series Walking with Monsters that deals with this. The wallpaper shows Arthropleura, a myriapod. On the scale picture to the right, it is the bottom right animal. All animals on that diagram are to the same scale – it was ~2 m. For a terrestrial arthropod, that is huge.

The largest animal on that diagram, on the left, is Jaekelopterus, a eurypterid (sea scorpion). It was the largest arthropod to have ever lived, but given that it's a marine animal, it is easier for it to reach large sizes.

On the top right, you see an insect. Remember that this is all on the same scale...

Diagram source: Braddy, S. J., Poschmann, M. & Tetlie, O. E. 2008. Giant claw reveals the largest ever arthropod. Biology Letters 4, 106-109. DOI: 10.1098/rsbl.2007.0491

It is an extinct dragonfly relative (Protodonata) with a 70 cm large wing span – by far the largest flying insect. See the embedded picture, bottom left, for a visual.

Note that in some popular articles, there are mentions of 2 m large protodonates. These are probably mix-ups with Arthropleura. The 70 cm ones are the largest.

Of course, this needs to be explained. Such terrestrial arthropod gigantism is unprecendented (and never repeated!). The explanation is a combination of environmental factors and physiological ones.

The Carboniferous was a time of maximal oxygen levels in the atmosphere (> 30%; today is 21%). Insects and myriapods take in oxygen mostly by diffusion (newest research is showing some very slight role of active breathing, but this is negligible) through trachaea, basically holes in their body. This is the major limitor of size – grow too large, and there is not enough oxygen being funnelled in.

What about the vertebrates? Terrestrial vertebrates can be broadly split into two groups: the batrachomorphs and the reptiliomorphs.

The batrachomorphs include the amphibians, and the earliest fossil representatives are a paraphyletic grouping termed the Temnospondyli, who were dominant in the Carboniferous (died out in the Early Cretaceous). They have a characteristic skull shap, being low with a round snout.

They were highly diverse, with some being amphibious (crocodile-like lifestyle), while others were completely terrestrial. However, all of them had to go back to the water to reproduce. This restricted their geographical range.

The other great terrestrial vertebrate group is the reptilomorphan one, which includes the dinosaurs, mammals and their ancestors. Many of them were aquatic and amphibious, while some were completrely terrestrial.

However, at some point, they developed a key innovation: the amniotic egg. This allowed them to be free of the restriction of having to go back to water to reproduce, allowing them to lay eggs in any environment, thus allowing them to expand greatly.

The earliest amniote is Hylonomus from the mid-Carboniferous.

The amniotes (i.e. the Reptilia) radiated in the late Carboniferous into three sublasses (left to right): the Anapsida, Synapsida and Diapsida. The differences between them are in the number of holes at the back of the skull (technical term: fenestrae, lat. "windows"): anapsids (representing the ancestral condition, as well as the turtles have none); synapsids (mammals) have one; diapsids (dinosaurs and lizards) have two.

How they later fared will be dealt with later. Now we have to return to plants again.

At the end of the Carboniferous, a new group of trachaeophyte evolved and rashly radiated: the gymnosperms.

The reason for this radiation is climatic changes. The Late Carboniferous climate was in many ways similar to today, except for the extraordinarily high oxygen concentrations. But besides that, it was an icehouse climate with biomes spread at around the same latitudes as today.

However, the transition to the Permian is marked by warming and the spread of aridity. The great coal swamps disappeared and were replaced by deserts. Thus, those plants that were free of the need for water to reproduce had a distinct advantage; the gymnosperms had that, as they produce seeds, which are the plant equivalent of the amniotic egg.

While the earliest true gymnosperms evolved in the Late Carboniferous, we can trace the stem group back to the Devonian, with Archaeopteris (not to be confused with Archaeopteryx!) being the earliest gymnosperm-like plant.

As I mentioned earlier, the tropical swamps were just one biome. The earliest gymnosperms of the Carboniferous (lumped together as paraphyletic "pteridosperms"), such as Glossopteris, were already widespread in the temperate and arid areas of Carboniferous landmasses.

With the end-Carboniferous climate changes, they were free to spread out and achieve geographical dominance.

The one group of gymnosperm that was especially selected for was the conifers – pine trees et al. Conifers are especially adapted for dry climates, especially through their needle-like leaves which minimise water loss. They were the group into whose hands (metaphorically-speaking, of course) the climate changes played, and they experienced their great radiation in the Early Permian.

Some representatives of these early conifers are shown above. Cordaites was especially common, as were the Voltziales, a now-extinct taxon. In both, you can see the distinct conifer leaves.

Voltziales picture source: Hernandez-Castillo, G.R., Stockey, R. A., Mapes, G. & Rothwell, G. W. 2009. A New Voltzialean Conifer Emporia royalii sp. nov. (Emporiaceae) from the Hamilton Quarry, Kansas. International Journal of Plant Sciences 170, 1201-1227. DOI: 10.1086/605874

So how did the vertebrate life react to these climate and vegetation changes? The (most likely) paraphyletic "pelycosaurs", are synapsids that were relatively diverse in the Carboniferous and Permian. They're childhood favourites because of the "sail" on their back, best known from Dimetrodon, but this is rather unique for the later pelycosaurs – most were small and insectivorous.

In the Late Permian, they experienced their own radiation...

… the result of which was these: the Therapsida. They had diverse lifestyles, with carnivorous gorgonopsians with wolf-like bodies and saber teeth; on the other hand, there were herbivores, like the dicynodonts.

However, they all died out at the end of the Permian, soon after they originated. This is through no fault of their own – over 90% of all life on Earth died out along with them in the most severe mass extinction event in the history of life on Earth.

The stats above say it all, as do the graphs, which come from a now-classic paper.

Source: Benton, M. J. 1995. Diversification and Extinction in the History of Life. Science 268, 52-58. DOI: 10.1126/science.7701342

To examine the P-T extinction, it is necessary to go back into the oceans, where the changes are much easier and accurate to map out.

In this diagram, what we see is that there was a dramatic shift in the taxonomic structure in the oceans of the Permian, with brachiopods being dominant in the mid-Permian, but then giving way to gastropods and bivalves by the Late Permian.

Diagram source: Bottjer, D. J., Clapham, M. E., Fraiser, M. L. & Powers, C. M. 2008. Understanding mechanisms for the end-Permian mass extinction and the protracted Early Triassic aftermath and recovery. GSA Today 18, 4-10. DOI: 10.1130/GSATG8A.1

Looking at this in more detail [sidenote: these diagrams contain a lot of data and are extremely informative. Look at and study them carefully!], we notice that in the Late Permian, the bivalves managed to disperse into slightly deeper waters (accompanied by gastropods, who had now evolved novel ways of locomotion), thereby pushing the previous occupants (bryozoans, brachiopods) into even deeper waters of the continental slope.

And the effect of the extinction can be seen here: stenolaemate bryozoans, which were relatively diverse in the Permian, were drastically reduced at the start of the Triassic and only achieved some semblance of recovery by the Late Triassic.

In fact, diversity in all marine groups took a long time to recover – over 6 Ma. This is in contrast to other mass extinction events, where recovery doesn't take longer than 1 Ma. This is not only seen in the actual fossil record, but also in the carbon isotope record, as detailed above. It took a long time for the carbon isotope fluctuations to return to regular levels.

Diagram source: Galfetti, T., Bucher, H., Brayard, A., Hochuli, P. A., Weissert, H., Guodun, K., Atudorei, V. & Guex, J. 2007. Late Early Triassic climate change: Insights from carbonate carbon isotopes, sedimentary evolution and ammonoid paleobiogeography. Palaeo3 243, 394-411. DOI: 10.1016/j.palaeo.2006.08.014

Here is a summary of the effect of the P-T extinction on marine taxonomic diversity. • Bivalves benefitted the most, as did the gastropods.• Brachiopods were losers – although not as big losers as the trilobites, who were wiped off

the Earth• Bryozoans also lost out, as did the pelmatozoans (crinoids – who were thought to be extinct

until the 1950s!).

A whole slate of groups were given some freedom to diversify though.

Many reasons have been proposed throughout the years for the P-T extinction event, and it is obvious that there isn't any root cause.

Anoxia (lack of oxygen in the oceans) can play a role, as can euxinia (high sulphur, low oxygen), hypercarbonia (high CO2) and the release of methane clathrates.

On the climate scale, there was a reduction in oxygen levels at the end of the Permian, as well as very extensive volcanism and global warming. All of these were dynamically affecting each other – none of them act alone.

Extraterrestrial causes are always associated with any event in the history of the Earth, no matter how nonsensical. For the P-T, asteroid impacts have been proposed – with no evidence – as have more outlandish ideas such as gamma-ray bursts and supernova winds causing extreme irradiation. These are all evidence-less hypotheses.

One space-related factor that was brought to my attention in the Q&A session afterwards is the effect of Milankovitch cycles (see Ice Age section of last talk) or changes in the Sun's power output. These can play into the first two categories.

The most important thing to realise about the P-T extinction event is that it wasn't a sudden event. The faunal turnovers didn't happen at one point in time, they were gradual. This effectively rules out a disaster impact from space, as with the K-T event that wiped out the dinosaurs.

Instead, climate and environmental changes are generally slow to act out and that's where we must look.

It is in fact so that as of the Late Permian, anoxia started to creep into the oceans and gradually became more and more severe, eventually reaching a stage in the latest Permian when the entire oceans were anoxic, a stage that persisted into the earliest periods of the Triassic and gradually recovering, concurrent with the faunal recovery. This event is termed the P-T superanoxia event.

Diagram origin: Isozaki, Y. 1997. Permo-Triassic Boundary Superanoxia and Stratified Superocean: Records from Lost Deep Sea. Science 276, 235-238. DOI: 10.1126/science.276.5310.235

What can cause such an event? Global warming. And it is so that in the Late Permian, there was extremely intensive volcanism: look at the map above. All the purple is lava and other volcanic material deposited in a short period in the Late Permian in Russia.

Increased volcanism leads to more carbon dioxide being released in the atmosphere, as well as other gases, including sulphides. The carbon dioxide leads to hypercarbonia and ocean acidification, as well as global warming. The sulphides lead to acid rain, wreaking havoc on land.

And here is a flow diagram of the whole ordeal.

And to think that this all began with some extra release of carbon dioxide... Sound familiar?