Extreme evolution

Like most things in biology, we can only truly understand the nature of extreme organisms and extreme environments in the context of their evolution. The conditions we observe today are but a snapshot in time and the organisms are a product of a long history of change, both in themselves and in the conditions which surround them. Conditions on the early Earth were very different from what they are today. It is in this context that we need to consider the nature of extreme organisms and environments. However, before I consider how an evolutionary perspective can shed light on our understanding of this area, let us look at one of the best studied examples of evolution in an extreme environment.

Frigid fish: a case study of evolution in an extreme environment Notothenioid fishes dominate the fish fauna of Antarctic coastal waters. They make up 55 per cent of the species and 90 per cent of the individuals that are caught there. Their success in Antarctic waters is attributed to a single adaptation - the evolution of antifreeze glycopro-teins. Although they face a number of problems in cold Antarctic waters, they could not persist there without a mechanism for preventing the ever-present risk of the freezing of their blood (see Chapter 5). They are thus a unique example of evolution in an extreme environment that can be attributed to the development of a single protein. After the fragmentation of Gondwanaland, Antarctica gradually drifted south, cooling as it did so. This represented a cooling of surface waters from about 20 °C down to the temperature seen today (—1.9 °C). Antarctica became isolated by the development of the Antarctic Circumpolar Current during the early Oligocene to early Miocene (38-25 million years ago - the Cenozoic Era, see Figure 7.1). This resulted in the cooling of Antarctic waters and antifreeze glycoproteins must have evolved by the mid-Miocene (about 17 million years ago). This is relatively recent in terms of evolutionary time, and means there is some chance of deciphering the evolutionary processes that occurred. Coastal fish living in Arctic and northern temperate waters are faced with similar problems and have developed similar antifreeze proteins.

Chi-Hing Cheng and Liangbiao Chen working in Professor Arthur DeVries's research group at the University of Illinois-Urbana have been unravelling the evolution of the genes responsible for producing antifreeze proteins. Antarctic notothenioid fish produce several different types of antifreeze glycoproteins (proteins with attached carbohydrates). Antifreeze glycoproteins are also produced by cod (Gadidae) from cold waters in the northern hemisphere. Other groups of fish produce antifreeze proteins (without the attached carbohydrates). Four different types of antifreeze proteins have been described. These are found in groups of fish that are only distantly related to one another or to the Antarctic notothenioids. This suggests that antifreeze proteins

(or glycoproteins) have evolved independently among unrelated groups of fish several times. This is a striking example of convergent evolution - the development of a similar solution to an environmental stress by unrelated groups of organisms. A number of groups of fish living in coastal polar or northern temperate waters have independently evolved different types of antifreeze proteins and glycoproteins that protect them against the risk of freezing.

Cheng and Chen have determined the structure of the gene responsible for the production of the antifreeze glycoprotein of an Antarctic fish. They compared this gene structure with those of other genes, the sequences of which are stored in computer databases. The antifreeze glycoprotein turned out to be similar to one end of the gene sequence coding for trypsinogen from plaice (a flatfish). Trypsinogen is one of the steps in the production of the intestinal enzyme trypsin, which is a protease involved in the digestion of the proteins contained in the animal's food. This suggests that the fish antifreeze glycoprotein evolved from a gut enzyme, an example of an existing gene becoming modified to produce a protein with a new function. Ice crystals are continually being ingested by the fish along with food and water. The gut is thus a major site of potential ice nucleation and it is perhaps not surprising that a gut enzyme has become modified to deal with this threat. Cheng and Chen have now isolated a gene that represents an intermediate in the process; this produces both an antifreeze glycoprotein and a trypsinogen-like protease. Antifreeze glycoproteins that circulated in the blood, and other body compartments, must have developed from those which were secreted into the gut.

Genes contain sequences (exons) that code for proteins separated by non-coding sequences (introns, sometimes called 'junk' DNA since such sequences do not code for the production of proteins). The region of the trypsinogen gene that shows similarity to the antifreeze glyco-protein gene includes part of the non-coding sequence. Antifreeze gly-coproteins thus owe their origin to 'junk' DNA and are examples of sense being created out of nonsense. This is a very rare demonstration of this method of evolving new genes. Using molecular clocks (changes in molecules whose rate of evolution is known), Cheng and her coworkers have determined that antifreeze glycoproteins evolved between 5 and 14 million years ago. This corresponds to the time that Antarctic waters cooled to freezing temperatures. By developing this molecule that enabled them to survive in Antarctic waters, nototheni-oid fish were able to fill the niches vacated by fish that were unable to survive the conditions created by the cooling of Antarctica.

The sequence of amino acids from the antifreeze glycoprotein of the Arctic cod (Boreogadus saida) is almost identical to that from an Antarctic notothenioid (Dissosticus mawsoni). These two Arctic and Antarctic groups are thought to have been isolated from each other for about 40 million years, long before the cooling of Antarctic waters and the evolution of the antifreeze gene. Differences in the structure and organisation of the antifreeze genes from the two fish reveal their separate evolutionary origins. No regions of the Arctic cod gene bear similarity to trypsinogen (unlike the Antarctic notothenioid antifreeze gene) and the gene appears to have had a different origin. Four different types of antifreeze proteins have been described in a number of groups of fish inhabiting polar and northern temperate waters, including some sculpins, sea ravens, eel pouts, wolf fish, smelt, herrings and winter flounder. The presence of antifreeze proteins in unrelated groups of fish indicates that the genes responsible for their production evolved independently. Antifreeze proteins are also found in terrestrial arthropods, plants and molluscs, and there is evidence of their presence in nema-todes. They are found in situations where it is important for the survival of the organism to either prevent freezing or to control the size, shape or location of ice crystals in their body. The evolution of antifreeze (or ice-active) proteins thus represents a widespread response to the risk of freezing in environments where extreme cold is experienced.

What is extreme: an evolutionary solution?

The life box definition of an extreme organism, proposed in Chapter 1, considered that such an organism could survive environmental conditions beyond those tolerated by the majority of organisms (see Figure 1.3). However, the conditions tolerated by organisms have changed. This is both because conditions on Earth have changed throughout its history and because the organisms themselves have evolved new abilities that enable them to live in places where they could not live before. Let us look at a few examples.

Life began in the sea and organisms had to solve a number of problems to move from an aquatic to a terrestrial environment. The land was probably first colonised by microorganisms. They would, however, have been restricted to habitats that were, at least periodically, wet. Microbes cannot grow unless they are immersed in water. Their ability to survive in an anhydrobiotic or dormant state would, however, have seen them through the dry periods. Plants colonised the land during the mid-Silurian period (420 million years ago, see Figure 7.1). They are thought to have evolved from green algae and needed to develop a waxy cuticle and stomata, to control desiccation, and roots to acquire water and nutrients and to anchor them to their substrate. Animals did not colonise the land until after the plants since they needed them for food and, perhaps, shelter. Arthropods (particularly spiders and insects) started to colonise the land about 410 million years ago and vertebrates (leading to the development of amphibians, reptiles, birds and mammals) about 374-360 million years ago.

Animals had to solve a number of problems to make the transition from a fully aquatic (living in water) to a fully terrestrial (living in air) lifestyle. Air is much less dense than water and so they needed some sort of skeleton to support their bodies. Terrestrial animals have to face much greater temperature extremes since they have forgone the thermal buffering properties of water. Marine animals can fulfil their requirements for water and salts from the seawater surrounding them, whereas terrestrial animals must acquire them by eating and drinking. Terrestrial animals must also maintain their water content in an often dry environment.

The problems of life on land were solved long ago and terrestrial organisms have since colonised every possible habitat on land. We do not think of most terrestrial habitats as being extreme, but, to an organism living in the early Silurian period, all terrestrial habitats would have seemed extreme (if it had been capable of thinking about it). At that time, the life box of the majority of organisms would have encompassed the conditions that were found in the sea, and perhaps some other aquatic habitats. The life box of a terrestrial organism would have lain outside the life box which encompassed those of the majority of organisms and hence the terrestrial organism would be considered to be an extreme organism, for its time. Terrestrial organisms have now become so numerous that the life box of the majority of organisms embraces most terrestrial conditions and they are no longer extremists. The recognition of extreme conditions and extreme organisms changes as conditions and organisms have changed.

As well as organisms changing to colonise an extreme environment (as in the movement from water to land), there have been dramatic changes in the conditions on Earth which have required organisms to change or become extinct. The early Earth had an anaerobic atmosphere, lacking in oxygen. The concentration of oxygen in the atmosphere only increased after the evolution of photosynthetic organisms, which produced oxygen as a product of their photosynthesis. Such organisms are thought to have evolved before 2.5 billion years ago (see Figure 7.1). Oxygen levels in the atmosphere would not have risen, however, until most oxidisable materials on the Earth had been exhausted. Iron and some iron minerals are unstable in the presence of oxygen (like a rusting nail, for example). The deposition of iron minerals in sedimentary rocks indicates that the absorption of oxygen by oxi-disable minerals was complete by about 1.7 billion years ago. There was thus a fundamental change on Earth from anaerobic (no oxygen) to aerobic conditions (oxygen present in the atmosphere). Early organisms were anaerobes; to them, exposure to oxygen represented extreme conditions since they could not survive exposure to its toxic products. Organisms evolved that could cope with the aerobic conditions. Those that did not acquire this ability either had to survive in the few remaining anaerobic environments, or they became extinct. In the ancient anaerobic world, the aerobic organisms were the extreme organisms, but, now that aerobic conditions are prevalent, it is the anaerobic organisms that are the extremists. What once was extreme has become normal and what once was normal has become extreme.

Many researchers now conclude that, as well as being anaerobic, early organisms were thermophiles or even hyperthermophiles, living at much higher temperatures than are considered normal on Earth today. As the Earth cooled, organisms evolved which could survive and function in the cooler conditions. Hyperthermophiles are still with us today, but, at the Earth's surface, they are restricted to the relatively rare habitats of hot springs and hydrothermal vents that provide the high temperatures to which they are adapted. Organisms living deep below the surface of the Earth (see Chapter 2 - The underworld) also live at high temperatures and are widespread, with a total biomass perhaps exceeding that at the surface. Maybe these hyperthermophiles retreated to their subterranean world as the surface cooled, or perhaps life evolved there in the first place.

Is the deep sea extreme?

The deep sea is widespread. The seabed, covered by more than 3000 metres of seawater, makes up 53 per cent of the total surface of the Earth. The deep sea is likely to have been present for most or all of the time that organisms have been present on the Earth. For organisms that evolved in surface waters, life in the depths presented a number of problems. In particular, organisms which colonised the deep sea had to develop mechanisms for coping with the high pressures that are found there (see Chapter 6, Under pressure). A wide diversity of invertebrate animals inhabit the deep sea (see Chapter 2, The cold deep sea) and it is likely to have been colonised at different times by different groups of animals. Fishes are probably the most recent colonisers, with 10-15 per cent of fish species living there.

The deep sea clearly represented a challenge to its colonisers, but it also provided an opportunity. As a whole, it is the largest environment on the Earth's surface. It is supplied with food via the dead bodies, and other products, of organisms from surface waters. We might think of the colonisation of the deep sea as being comparable to the colonisation of the land. It was once an extreme environment, but, just as we would not now consider most terrestrial environments to be extreme, such a wide diversity of organisms have solved the problems of living in the deep sea that we cannot now consider it to be extreme. Once the problems of living in a widespread environment had been solved, colonising organisms would also have become widespread and developed into a diversity of species. They are encompassed by the life box of the majority of species. In other words, the life box of life on Earth has expanded with time. Some extreme environments, however, are rare and are likely to have been rare throughout the history of the Earth. Examples include salt lakes and extreme acidic or alkaline conditions. Organisms that colonise these environments will remain rare and their status as extreme organisms will not change. However, not all rare habitats are extreme. Extreme habitats are those whose physical conditions (temperature, salinity, water availability etc.) lie outside those experienced by the majority of organisms.

Pioneers and stragglers

We can envisage how extreme environments and extreme organisms have changed with time by considering how their life boxes, and the life box for life on Earth in general, have changed (Figure 8.7). We might recognise three situations: the first two involve extreme organisms being pioneers and the third involves them being stragglers. Extreme organisms that are pioneer colonists of a new (and extreme) but widespread environment will no longer be considered extreme once the problems of living in that environment have been solved and its colonisation has become widespread (Figure 8.7A). Pioneer colonists of rare extreme environments are likely to remain rare and extreme (Figure 8.7B). If the average conditions on Earth change, those organisms which do not adapt to the new conditions (the stragglers) may be able to survive in the now rare and extreme environments that retain the old conditions (Figure 8.7C). The life box can thus give us a way of recognising extreme organisms, but only if we realise that the situation is dynamic.

figure 8.7 Three possible models for the evolution of extreme organisms. Open circles represent organisms that have changed to a new set of conditions, while closed circles represent those which have retained an old set of conditions. Those conditions and organisms which lie outside those of the majority are considered extreme.

In (A), the extreme organisms are pioneer organisms colonising an extreme but widespread environment (such as the land or the deep sea). As the problems of living in the new environment are conquered, organisms become widespread in this environment and can no longer be considered extreme, since their life boxes are encompassed by those of the majority of organisms.

In (B), the extreme organisms are pioneer organisms colonising an extreme and rare environment (such as salt lakes). The environment remains rare and the organisms continue to be considered extreme.

In (C), the conditions on Earth have changed (as in the change from anaerobic to aerobic conditions). Most species have evolved to survive in the new conditions and many have become extinct, but the stragglers survive in the now rare and extreme environments which retain the old conditions.

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