The origin of life on land

When they went ashore the animals that took up a land life carried with them a part of the sea in their bodies, a heritage which they passed on to their children and which even today links each land animal with its origin in the ancient sea.

Rachel Carson, The SeaAround Us (1951)

All life came from the sea, and it's not just the animals that carry some of that water-living heritage: plants do too. The classic story is that plants emerged from the watery depths perhaps in the Silurian or Devonian period, some 400 million years ago, and these were followed soon after by insects and worms, and other small animals that could find new places to live and feed among the branches of the simplest land plants. These small creeping things were then followed by the first vertebrates on land, when some hefty fishy creature dragged itself over the waterside mud and started to eat flies.

As ever, the reality is rather more complex, and new fossil discoveries have pushed the origin of land life back much further in time than had been imagined. Indeed, there may well have been some simple microscopic photosynthesizing organisms around the fringes of the seas and lakes even in Neoproterozoic times. But does it really matter when life moved onto land ('conquered the land' in the old phrase)? Perhaps we are just interested because we are land-livers? In fact, life on land is hugely significant for two reasons.

The first reason is that life on land represents most of modern biodiversity. Whereas some 500,000 species live in the sea today, at least ten times that number live on land. The bulk of modern biodiversity consists of insects, but other terrestrial groups, like other arthropods (spiders, centipedes), as well as flowering plants are much more species-rich than anything in the sea. So life has really prospered after it moved onto land.

Second, life has changed the face of the Earth. Before there was life on land, there were no soils. The Earth's surface was barren rock, and rates of erosion were vast, more than ten times what they are today. Mountains were rocky crags, and lowland plains were dustbowls. As life moved onto land, soils developed (soil is

5 just rock dust plus organic matter), and the soils and plants crept o t outwards from the water and covered more and more of the o

| surface. But did this process really begin in the Neoproterozoic?

Precambrian mushrooms

When molecular biologists presented evidence that some plant groups existed 600 million years ago, palaeontologists were outraged. This proposal pushed the record of land plants back by 200 million years. However, there are indeed some excellent fossils of some possible lichens from rocks of that age. Lichens are symbiotic (mutually beneficial) associations of a fungus with a green, photosynthesizing organism, usually an alga or a cyanobacterium.

Then Precambrian lichens were reported in 2005 from the late Neoproterozoic rocks of Doushantuo in China, a remarkable source of exceptionally well-preserved fossils of extraordinary age. The specimens are so well preserved, even to cellular level, that most palaeobotanists are convinced by the new finds. It had long been suspected that cyanobacteria formed thin crusts on land, as they do in desert regions today, photosynthesizing and forming thin 'soils' in the Proterozoic. The oldest fossil soils, dated at 1.2 billion years old, were presumably generated by microbial or algal activity. The Doushantuo lichens prove that the surface of the land, at least close to the water, was already green at the end of the Precambrian, long before plants really conquered the land.

But of course, lichens are fungal associations and fungi are not plants (see p. 36). So, the molecular results that suggest a Precambrian origin for green plants are still highly disputed. True plants apparently did not move onto land until later.

Green plants on land |

The land began to become green in the Ordovician, some f

450 million years ago. The first land plants seem to have been e o bryophytes, commonly called mosses and liverworts. The oldest a recorded fossil bryophytes are Ordovician in age, although d interpretations are uncertain, and there is a possible Cambrian relative, Parafunaria from China.

There are additional hints that green plants were moderately diverse, at least in some locations, in the Ordovician. For example, Ordovician soils with root-like structures suggest that plants were already on land. Something substantial then seems to have happened in the Mid Ordovician, when the character of microfossil assemblages changed dramatically: spores appeared. Spores are airborne microscopic cells that are characteristic of land plants. So, although these earliest land plants have not yet been found as fossils, they must have been there because they were producing spores. But the nature of these spores has been debated: whether they really came from green plants, or might simply be the products of green algae.

In 2003, Charlie Wellman from the University of Sheffield showed that the Ordovician spores were probably produced by small bryophytes, perhaps like liverworts. He found detailed similarities in the spore walls to those of modern liverworts, and he also found clusters of spores packaged in a type of cuticle that looked overall like a liverwort spore-bearing organ.

Bryophytes today show special adaptations to life on land, such as a waterproof cuticle over their leaves and stems. Many also have stomata, specialized openings under the leaves used for controlling water loss. Some bryophytes have the unusual ability to dry up completely, and then to re-hydrate when rain falls, and continue as normal. It seems then that low-growing mossy plants invaded the land in the Ordovician, and that larger green plants came later.

f Adapting to life on land x

¡= As humans, for whom swimming is a bit of a struggle, we would naturally think that the key challenge for a water-dweller on land is breathing. However, breathing air, as opposed to extracting oxygen from the water, was in fact the least of the problems of the earliest land animals. And for plants, the challenges are obviously rather different. They relate especially to obtaining nutrients and water, prevention of desiccation, and support.

Nutrition first. In water, a plant may absorb nutrients and water all over its surface, but on land, all such materials must be drawn from the ground, and passed round the tissues internally. Land plants typically have specialized roots that draw moisture and nutrient ions from the soil, which are passed through water-conducting systems that connect all cells. The system is driven by transpiration, a process powered by the evaporation of water from leaves and stems. As water passes out of aerial parts of the plant, fluids are drawn up into the water-conducting system hydrostatically.

Water loss is a second key problem for plants on land. Whereas in the water, fluids may pass freely in and out of a plant, land plants are covered with an impermeable covering, the waxy cuticle. Gas exchange may be controlled by specialized openings, the stomata (singular, stoma), often located on the underside of leaves, and as seen in some bryophytes. Typically, stomata open and close depending on carbon dioxide concentration, light intensity, and water stress.

The third problem of life on land is support. Water plants simply float, and the water renders them neutrally buoyant. Most land plants, even small ones, stand erect in order to maximize their uptake of sunlight for photosynthesis, and this requires some form e of skeletal supporting structure. All land plants rely on a §.

hydrostatic skeleton, a stiff framework supported by water in f tubes, and some groups have evolved additional structural support e o by the deposition of the tough organic polymer lignin on the a internal fibres and canals of the trunk. d

The first vascular plants

The oldest known vascular plant is Cooksonia from the Mid Silurian, some 425 million years ago, of southern Ireland, a genus that survived for some 30 million years. Cooksonia (Fig. 12) is composed of cylindrical stems that branch in two at various points and are terminated by cap-shaped spore-bearing structures at the tip of each branch. The specimens of Cooksonia range from tiny Silurian examples, only a few millimetres tall, to larger Devonian forms up to 65 millimetres tall.

In lifelong studies of these extraordinary little plants, Dianne Edwards of the University of Cardiff has discovered spores in the

12. Cooksonia spore-bearing organs, the presence of thickened walls of the vascular conducting tissues, and stomata on the outer surfaces of the stems. All these discoveries were won against considerable odds: much of the material is incomplete, and it all has to be processed through several elaborate protocols.

While stands of Cooksonia in the Silurian perhaps reached a height of 6 centimetres at most, little more than roughly cut grass, vascular plants became rather larger in the Early Devonian, 400 million years ago. These Early Devonian terrestrial settings are best known from an extraordinary fossil locality in Scotland, the famous Rhynie Chert. The locality is remote, but when fossils were first found there in 1914, they soon attracted intense attention. Not only were these some of the oldest plants yet found, but they were also diverse, and exquisitely well preserved. Further, here and there among the stems and stalks were small arthropods and other animals.

The Rhynie fossils have been preserved by flash silicification by hot springs. Recent work by Nigel Trewin and Clive Rice from the University of Aberdeen has shown that much of Scotland was an active volcanic zone at the time. Rhynie in the Early Devonian was like Yellowstone National Park today, with hot geysers erupting and immersing vegetation in silica-rich waters at a temperature of 35 °C - an ecosystem frozen (or rather boiled) in time. The Rhynie Chert is an unusual, hard, flinty rock, speckled black and white. The fossils cannot readily be seen on the surface, and they have to be studied in cross-sections cut through the rock, polished to an exquisite thin lamina on a microscope slide, and examined at high magnification. e

The Rhynie fossils include remains of seven vascular land plants, f as well as algae, fungi, one species of lichen, and bacteria, as well e o as at least six groups of terrestrial and freshwater arthropods. a

What is amazing is the quality of preservation: every cell and fine d detail can be seen, as if frozen in an instant and preserved forever.

The Rhynie ecosystem was no towering forest. If you went for a stroll in Scotland in the Early Devonian, the green rim of plants probably did not extend far from the sides of ponds and rivers, and the tallest plants would barely have brushed your knees (Fig. 13). To see anything, you would have had to go down on your hands and knees, and peer at the stems through a magnifying glass. Most of the taller plants had smooth stems, and branched simply in two, with knob-like spore capsules at the tops of their stems - just larger examples of plants like Cooksonia. Asteroxylon had small scale-like leaves growing up from the stem. Microscopic cross-sections of these plants show they had simple vascular canals, stomata, and terrestrial spores. Between the plants crept spider-like trigonotarbids and insect-like arthropods, and some of

¡= these are even found within cavities in the plant stems. There were crustaceans in the warm pools.

Through the remainder of the Devonian, mosses and other bryophytes lived in damp places, and did not seem to change much. But the vascular plants were evolving fast. They occupied spots further and further away from the waterside. The Rhynie plants all had their toes in the water, being connected to horizontal rhizome systems at the base, and the rhizomes were probably generally beneath water or damp mud. As the Devonian progressed, more and more vascular plants evolved their own root systems, and so were less dependent on standing water. The roots sought moisture at depth, and water permeated the plant through transpiration. These changes enabled the later Devonian plants to become larger than mere reeds, and some were positively tree-like by the end of the period, just before the time of great rainforests, the Carboniferous (see p. 87).

Scurrying through the undergrowth

Palaeontologists have hunted actively for evidence of animal life on land in association with the Ordovician and other very early soils and spore accumulations. So far, no luck. But there is some intriguing evidence that quite large animals actually moved on land at this time. In 2002, Robert MacNaughton from the Geological Survey of Canada, and colleagues, reported some large tracks produced by arthropods in desert-like sandstones dated as latest Cambrian or earliest Ordovician. These tracks are up to 29 centimetres wide, and they show symmetrical V-shaped markings probably formed by the back end of the animal, perhaps some sort of mollusc or worm that ploughed through the surface sands. An animal of such a size on land in the latest Cambrian is a real surprise!

3"

The oldest body fossils of land animals come from the Late §.

Silurian of Scotland and the Welsh Borders of England. In a f series of studies, Paul Selden of Manchester University, and e o colleagues, have identified numerous land-living arthropod species a from cuticle fragments. The fossils are microscopic, and they d occur in black, organic-rich mudstones, and are not immediately obvious. The researchers break up the sediment, treat it with acid, often hydrofluoric acid, in order to break down all the sand grains and non-organic detritus. They can then pick through the plant and arthropod cuticles under the microscope. These studies were a huge surprise, because Selden and colleagues were able to extract diagnostic elements that matched bits of modern arthropods -pieces of legs, head shields, body segments, and other detritus.

The earliest land-living arthropods include millipedes and trigonotarbids. Millipedes are familiar enough today, but trigonotarbids are less well known. These are extinct spider-like arthropods, with eight legs (like modern spiders), and some at least could probably spin silk from spinnerets located at the back of the abdomen (also like modern spiders). Trigonotarbids did not have the narrow constriction between the abdomen and head portion, as seen in spiders, but a more straight-sided beetle-like body. Trigonotarbids were hunters, and they apparently lurked in and around the earliest plants awaiting their prey.

As mentioned above, the Rhynie Chert, somewhat younger, has also proved to be a rich source of early land animals (Fig. 13). The cherts have produced millipedes and trigonotarbids, as seen in the Late Silurian localities, but also shrimps and collembolans. Collembolans, more commonly called springtails, are strange little creatures, close to being insects, but not quite, that have a forked structure under their belly that is bent forwards. If threatened, the collembolan can release the fork and it propels the animal through the air for up to 80 times its own length in a split second - a good defence against a doubtless startled trigonotarbid or spider.

5 By the Middle Devonian, some additional modern arthropod o t groups had appeared. The Gilboa locality in New York State has | produced fossils of millipedes, trigonotarbids, and mites, as well as ¡= the first insects and spiders. Scorpions are known from freshwater deposits before this time, but the first terrestrial forms occur in the Middle Devonian. Other arthropods from these sites include the long-legged predatory chilopods and the detritus-eating diplopods.

The Late Silurian and Devonian terrestrial ecosystems were different from today. The arthropods were mainly detritus-eaters and carnivores, with very few, or no, herbivores. Herbivory requires specialized gut microbes that can digest cellulose and lignin from plants, and this capability does not seem to have existed in the Silurian and Devonian. This is such a difference from modern arthropod communities, which are dominated by insects, and in which there are numerous forms that eat leaves and wood - think of all the larvae that eat plants in the garden and termites that can eat a wooden house in weeks!

So far we have seen life close up among the undergrowth. The arthropods of Silurian and Devonian times were all small, only a few millimetres in length. They were accompanied by worms and snails, although fossil records of these groups are sparse. Sooner or later, however, something larger was bound to make its ponderous way onto land and start eating all these nutritious little worms and arthropods.

The first tetrapods

Vertebrates may be divided loosely into fishes and tetrapods. Fishes have fins and swim in the water, and tetrapods (literally 'four feet') have legs and walk on land. Modern tetrapods are the amphibians, reptiles, birds, and mammals, but the first tetrapods were quite different from anything now living. The transition from fish to tetrapod happened in the Devonian, a time when coral reefs e flourished in tropical seas, and fishes, many of them armoured, §. swam in shallow seas. Indeed, some of the Devonian armoured f fishes were quite astonishing - Dunkleosteus was a placoderm e o

('platy skin') that reached a length of 10 metres, and could have a engulfed anything in its vast jaws. Other fishes, though, had lungs d and muscular fins that were used for dragging their bodies along lake beds.

A remarkable discovery in 2006 shed new light on the transition from fish to tetrapod. Three skeletons were retrieved from Devonian rocks of Arctic Canada that looked like hefty fishes (gills, scales, streamlined skull), but had some tetrapod characters (powerful limbs with rotating wrist and ankle joints, mobile neck, weight-supporting ribs). This creature, named Tiktaalik, was clearly capable of hauling itself onto land and breathing air as it sought another pond.

The next step is seen in fossils from the Upper Devonian of Greenland, some 370 million years old, that came to light in 1929. These were later namedAcanthostega and Ichthyostega (Fig. 14).

& 14. Ichthyostega andAcanthostega reconstructions if v ■n i—

They both measure 0.5-1.2 metres long, and they were carnivorous, presumably feeding on fishes. Acanthostega and Ichthyostega retain a fishy body outline with a streamlined head and a tail fin. The skull is very like that of their fishy ancestors, being smoothly streamlined, and carrying lateral line canals. These structures are found in many Devonian fishes and in life presumably carried nerves and sensory organs that detected movements underwater. Modern fishes have such structures.

The main differences from fishes are seen in the limbs and the limb girdles. In fishes, the shoulder girdle attaches to the back of the skull, behind the gills. This strengthens the front ofthe body and provides a firm anchor for the pectoralfins, the front pair. In an animal that walks on land, having the shoulder girdle fused to the skull might cause problems: as the animal walked it would jolt its head all the time, and this would disturb its hearing and other senses (and might make it bring up its lunch). The pelvic girdle, the hip region, is fused to the backbone on each side, and this provides an even firmer anchor for the hind limbs.

The limbs of Acanthostega and Ichthyostega are the key to everything. As expected, they are just like our arms and legs - a single upper element, the humerus in the arm and the femur in the leg, a pair of lower elements in the forearm (radius and ulna) and shin (tibia and fibula), various wrist and ankle bones, and the fingers. But how many fingers?

Mike Coates and Jenny Clack, at the University of Cambridge, had a surprise when they prepared the hand region of one of their specimens of Acanthostega in the 1990s: they found that it had eight fingers. They then investigated the hindlimb, and found that e it had eight toes. The classic specimens of Ichthyostega actually §. showed seven fingers and toes, and Tulerpeton, a relative from f

Russia, has six. e o

So this means that five digits are not fundamental to tetrapods. d Humans have made much of the pentadactyl (five-digit) hand and foot - indeed it's the basis of the decimal system. Had we retained eight, seven, or six digits, perhaps our mathematics would be rather different. And, as for pianos and clarinets, who knows? Coates and Clack were very clear about what this meant: there is nothing fundamental about five digits, and indeed modern work in developmental biology shows that this is true.

In development, a very early embryo has no limbs. Then small, featureless limb buds appear, the rudiments of the arms and legs. As the embryo grows larger, the limb buds extend and differentiate. The single bone of the upper arm and thigh appears first, then the double elements of shin and forearm, and finally the wrist and ankle elements. The fingers and toes pop out in sequence, but the numbers are not predetermined. The effects of different developmental genes, interacting with the tissues of the developing embryo, fix the number. So, early tetrapods experimented with many different numbers of digits, and five became more or less the norm by the end of the Devonian. But of course many tetrapods today have fewer (frogs have four, rhinos have three, cattle have two, and horses have one). No tetrapod with limbs has entirely dispensed with toes and fingers.

The Late Devonian tetrapods were still aquatic, as shown by the tail fin, lateral line system, and internal gills. The vertebral column was flexible, as in a fish, and Ichthyostega and Acanthostega could have swum by powerful sweeps of their tails. The limbs are still oriented more for swimming than walking, and the hands and feet, with seven or eight digits, are broad paddles. If this is true, and Mike Coates and Jenny Clack believe the case is very clear, we 5 have to look at the origin of terrestrial habits in tetrapods rather o t differently from the standard model (that is, fishes stepped onto | land and stayed there).

Mike Coates has argued that Acanthostega lived most of the time in stagnant, vegetation-choked backwaters, emerging in damp conditions, but staying underwater in the dry season and gulping air at the surface. It walked largely underwater, stepping over vegetation, and kicking itself along the bottom. So, it could be that these Devonian tetrapods had indeed stepped out of the water for a while, and then reverted to a somewhat more aquatic existence, or they might never have made the move completely onto land. This certainly happened in the Carboniferous, when tetrapods diversified and some became quite dedicated land animals.

Being a land animal...

Arthropods and tetrapods faced different challenges when they moved out of the water. For the tetrapods, the main problem was weight and structural support, whereas for the smaller arthropods, this was probably not much of an issue. In addition, both groups had to evolve new modes of locomotion as well as new ways of feeding, of sensing prey and predators, of water balance, and of reproduction. Air breathing, as mentioned before, was a relatively minor problem.

With all these problems, it might seem a wonder that animals bothered to depart the safety of the Silurian and Devonian waters and venture onto land. Alfred Sherwood Romer, the great doyen of mid-twentieth-century vertebrate palaeontology, argued that vertebrates moved onto land in order to get back into the water. This isn't such a paradox: he argued that the Devonian was a time of seasonal droughts, and the freshwater fishes probably found themselves often in stagnant and dwindling pools. Then, those that were able to gasp a few breaths in air, and haul themselves with effort along a watercourse to the next pool, would survive. e

The fishes that could not cope out of water then died. §.

Romer's idea has been criticized because there is actually only e o limited evidence of droughts in the Devonian (Romer was no a sedimentologist), and the 'getting back to water' model would not d explain why tetrapods continued to hone their land adaptations. It's more likely that the move to land by both arthropods and vertebrates was simply to exploit new opportunities. There were plants for the arthropods to hide in and whose detritus formed the base of a food chain. Once the arthropods were there, the tetrapods doubtless followed them and gorged themselves on juicy millipedes and trigonotarbids.

Structural support was the key issue for the first tetrapods, as mentioned. A fish is buoyed up by the water and its body weight is pretty much zero. On land, however, the body becomes heavy, and the belly has to be held clear of the ground if the animal is to move forward without wearing its ventral surface away. In addition, the internal organs weigh down within the rib cage, and there's a risk of suffocation or damage. The whole skeleton has to become modified to counteract gravity, to hold the guts in, and to allow the animal to hoist itself up and propel itself forwards.

Tetrapods move in a very different way from fishes in water. Instead of a smooth gliding motion driven by sideways beating of the body, the limbs have to operate in a jerky fashion, producing steps. The fishes most closely related to tetrapods are the sarcopterygians, or lobe-fins. Living sarcopterygians include the lungfishes of southern continents, and the famous 'living fossil' Latimeria, the coelacanth. Devonian sarcopterygians were a diverse group, and they all had muscular fins containing bones, and they could all have 'walked' on the bed of a pond by stilting themselves forwards. It then took only a moderate amount of evolution for the muscular fins of a lobefin to become an arm or a leg.

5 The earliest tetrapods also had to modify the ways in which they o t fed and breathed. The skulls of the ancestral sarcopterygian fishes

| were highly mobile, but this ability was largely lost in the early

¡= tetrapods. The jaw movements of tetrapods are much simpler than those of most fishes, and they could just snap at prey, and not chew it. Air-breathing requires lungs, but the sarcopterygians already had lungs. Lungfishes today can breathe with their lungs in the air, but they can also absorb oxygen from the water through their gills, and through other tissues in the mouth. Doubtless, the first tetrapods could respire in several ways also.

Sensory systems had to change too in the first tetrapods. The lateral line system could only be used in the water. Eyesight was as important on land as in shallow ponds, and the sense of smell may have improved, but there is no evidence of that in the fossils. Early tetrapods had a poor sense of hearing in air, as did their ancestors - we know this because their main hearing bone, the stapes, which connects the eardrum to the brain, was a rather massive rod of bone, and was surely not capable of discriminating subtle differences in sounds.

but only a partial solution

The first arthropods seem to have become more or less adapted to life on land at their first effort. They had waterproof cuticles, and some at least presumably laid their eggs on land. But this was not the case for the first tetrapods: they cracked most of the business of living on land, but left a couple of problems unresolved.

The first unsolved problem was the maintenance of water balance. In the air, water can evaporate through the moist skin of the body, the lining of the mouth and nostrils, and the early tetrapods risked desiccation. The earliest tetrapods probably remained close to fresh water, which they could drink in order to avoid this problem. Later, reptiles evolved waterproof scales and skins so they could escape entirely from the water, and still avoid desiccation in even the driest of conditions. The first tetrapods were certainly not capable of that.

Reproduction was the final hurdle to be crossed, and the first tetrapods, and amphibians today, made no evolutionary headway with this at all. Modern frogs and salamanders lay their eggs in ponds, and the young hatch as tadpoles. Tadpoles are really little fishes that live entirely in the water, and it is only after metamorphosis that the adult amphibian enters into a more terrestrial life, but even then only in a rather uneasy fashion. We know that early tetrapods had the same double mode of reproduction because a number of fossil tadpoles have been found. Again, it took some time before the reptiles came on the scene, and finally solved the terrestrial reproduction problem by producing eggs with shells that could be laid on dry land.

The Carboniferous Period followed the Devonian, and this was the time of the great coal forests. Not only were these the source of coal, and so of the industrial revolution and the modern world, the Carboniferous was also a time of rapid change in terrestrial ecosystems, and the world began to take on something like its modern appearance for the first time - but that is true perhaps only when viewed from a distance. In closer focus we might be startled by 2-metre-long millipedes, dragonflies as large as seagulls, and great trees that looked more like ferns than anything we are familiar with.

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