Figure 1: The gull and black. form a ring species. The ancestors, of both species originated in Siberia from where they spread east and west around the North Pole to form two chains of interbreeding subspecies. Only in northern Europe, where the ends of the chains merge (dashed line) do they not interbreed.
The Species Enigma New Scientist 13 Jun 98
THE latest estimates suggest that perhaps as many as 30 million species live on planet Earth, though only 1.5 million have so far been described. Many more millions have already been and gone, a few leaving fossil remains. But what exactly is a species? The term is used to classify both living and extinct organisms. For instance, the modern horse, known as Equus caballus, is distinguished from the mountain zebra, Equus zebra, and both are distinguished from the extinct Equus giganteus. The first name is the genus name, and the second, the species name (Box 1). Most biologists define a living species as a distinct reproductive group-a population of organisms which naturally mate in the wild to produce viable offspring. This is called the biological species concept (BSC) (Box 2). Though widely used, the BSC is a relatively recent idea, and only one of many interpretations of the word "species". Biologists have been arguing among themselves over the exact meaning of the term for the past two hundred years, and disagreements continue to this day All species definitions have been found to have their limitations. The BSC, for example, relies on a knowledge of reproductive behaviour, so it is impossible to apply it among fossil species.
Disappearing life Going extinct
BIOLOGISTS will agree, however, that biological diversity is now disappearing at rates comparable only with the handful of major extinctions that have occurred in the 3.5 billion years of life on the planethuman population growth, pollution and habitat destruction is largely to blame. Because species are perceived as a prime currency of biological diversity, how they are defined plays a crucial part in attempts to conserve life on Earth. For more than 2000 years, the ideas of the Greek philosopher Plato dominated scientists' views on species. Plato believed that the natural world was underpinned by "ideas" or "essences", of which individual animals and plants were imperfect copies. The species "type" was immutable. By the early 1800s, it was widely understood that fossils were the remains of ancient creatures. But while some fossils had no living relatives, others seemed to be primitive versions of living species. If species were immutable, what did this mean? Some writers explained the demise of these ancient species by sudden catastrophes, such as the Biblical flood, perhaps followed by the creation by God of new species. But in 1859, Charles Darwin offered, in his famous book On the Origin of Species, an explanation of fossils so compelling that it ended forever the notion of species as Godgiven and unchanging. After many years of study around the world, Darwin suggested that all living organisms arose from pre-existing forms through a slow and gradual process of change and modification-evolution by natural selection.
At any point in time, the characteristics of animals and plants might seem fixed and unchanging. But over thousands or millions of years, these characteristics were likely to be modified as organisms adapted to changes in their environment. Before Darwin, one of the problems confronting natural historians was how to interpret variation within species. Many species vary in size, shape or colour over their geographic range. House sparrows in North America, for example, are larger in the northern states than in the south. The terms variety, race or subspecies are used to describe this variation within a species. Before Darwin, local variants were thought of as imperfections in the underlying "essence", as deviations from the ideal. But to Darwin, the existence of variation was not a mistake, but the key to his evolutionary theory. Darwin observed that much of the variation seen among individuals is passed on to offspring. Those variants which were better adapted to their environment would leave more offspring. Varieties could be the basis for new species, especially if they became geographically isolated, or carried adaptations which allowed them to exploit new resources. Despite the title of his book, Darwin offered no concrete definition of species. Nor did he see a need to do so. For Darwin, varieties and species were relative termsabstract boundaries we impose on a world always in transition. As he wrote in On the Origin of Species: "In short we shall have to treat species in the same manner as those naturalists treat genera, who admit that genera are merely artificial combinations made for convenience. This may not be a cheering prospect, but we shall at least be freed from the vain search for the undiscovered and undiscoverable essence of the term species." Darwin's evolutionary ideas shifted species from an idealised concept to an arbitrary definition. They also forced those who classified the living world, known as taxonomists, to consider descent as an underlying principle. Taxonomists were no longer attempting to decipher God's essences, but identifying individuals with a shared evolutionary history. Despite this philosophical shift, in practice the business of defining species changed little. Defining species boiled down to finding those common features in a group of individual organisms which distinguished them from other groups of organisms. A hundred years ago, taxonomists would use morphological features-the shape, size and colour of organisms and body parts -to make their species distinctions. This view of species, as clusters of individuals physically distinct from other clusters, became known as the morphological species definition. The main problem with this approach is the question of how different two groups have to be before they can be called separate species? Since there is no absolute criterion governing the demarcation of the boundaries between species, taxonomists regularly indulged in minor skirmishes over what was, or what wasn't, a species.
Four species of Galapagos finchescan be distinguished by the length and depth of their bills. Each species is represented as a cluster of distinct points - a cluster of morphologically similar individuals.
Reproductive glue In the breeding
IN THE 1930s two American evolutionary biologists, Ernst Mayr and Theodosius Dobzhansky, both highly critical of the morphological species definition, introduced the BSC. By placing all living things into distinct reproductive units, they believed that the BSC would remove much of the ambiguity inherent in the morphological definition. The criterion was now simple. If a group of individuals could potentially breed together in the wild to produce fertile offspring, then they belonged to the same species. Reproductive compatibility was seen as the glue which maintained species integrity. An emphasis on reproduction and the life cycle would also help resolve a range of incidental problems that had dogged morphological species definitions, such as the obvious morphological difficulty of classifying a caterpillar and a butterfly in the same species, or males and females which were markedly different. Even Carolus Linnaeus, the founding father of modern taxonomy (see Box 1), was confused by the mallard duck, classifying males and females as distinct species. Morphological definitions had also missed the existence of "sibling species", natural populations which look morphologically identical but do not interbreed with one another. Sibling species occur in all groups of animals, but seem to be much more common in insects and other invertebrates. One celebrated case of confusion caused by morphological definitions and sibling species arose out of attempts to control malaria in Europe earlier this century.
What's in a name?
MODERN taxonomy owes a great debt to the Swedish botanist Carolus Linnaeus (17071778), who took on the onerous task of categorising and classifying all living things. Linnaeus's hierarchical system of classification, which persists to this day, set out to group similar-looking species into genera, genera into families, families into orders, and so on. Linnaeus also established the binomial system of nomenclature. Each species is given a scientific name consisting of two Latinised names, which are italicised or underlined, followed by the authority or organisation responsible for the name. Corvus frugilegus L., for example, is the scientific name for the raven. Corvus is the name of the genus, while frugilegus denotes the particular species. Other members of the genus include the crow, Corvus corone L. The capital "L' is an abbreviation for Linnaeus, who was responsible for the name. A third Latinised name following the species epithet denotes a subspecies. The crow, for example, is recognised as two distinct subspecies, the carrion crow Corvus corone corone L. and the hooded crow Corvus corone cornix L. Although common names like rook and raven are easier to remember, they differ between regions or countries. A formal system of naming ensures that information about animals and plants can be communicated worldwide without confusion.
At one time, it was thought that there was just one type of mosquito that carried malaria, Anopheles maculipennis. Various attempts made to control the disease by spraying insecticides on the mosquito populations had only limited success until it was realised that this single "species" was actually made up of six sibling species, only three of which transmitted the disease.
Hybrid hiatus Mules and tigons
THE BSC had immense conceptual appeal. But it introduced new problems of its own. If a species could only be defined if its members were shown to be reproductively compatible, the only way to finally prove the point would be to conduct countless breeding experiments and discover which hybrid offspring were sterile or stillborn. Mating a horse with a donkey produces a sterile mule, while crossing a tiger with a lion yields a sterile tigon. There are thousands of plants in which well defined varieties produce sterile offspring when crossed. But even if fertile offspring were produced in an experiment, did this have any relevance to what actually happened in the wild, where organisms might have little opportunity to interbreed because of differences in their behaviour or habitat? As a rule of thumb, biologists argued that if there were no naturally occurring hybrids in those areas where two similar organisms shared the same environment, then this was a good indication that they were "reproductively isolated". But when two populations are geographically separated, it becomes impossible to test their species status this way. This was not the only difficulty A definition which depended on the notion of interbreeding reproductive communities necessarily excluded fossils. The BSC also complicated the picture for species which normally reproduce asexually, that is without the exchange of genetic material between the sexes. This method of reproduction occurs widely in nature, and is very common among bacteria.
DNA to the rescue? Genetic distance
THE discovery of the DNA code revolutionised taxonomy Each individual organism inherits a sequence of nucleotide bases which is highly preserved from generation to generation. Chance changes in this code happen fairly infrequently, and if these genetic mutations are not damaging to the individual, they can be passed on to the next generation. A tree of mutations should give biologists the tree of evolutionary descent. Though this approach is complicated by the differences in rates of mutation between genes and species, and has failed to provide an ultimate arbiter on what constitutes a species, it is now adding immensely to our understanding of the relatedness of different populations. One recurring problem is that variability in DNA is often not correlated to variability in morphology or reproductive compatibility. Take the case of the chimpanzee Pan troglodytes and the pygmy chimpanzee or bonobo, Pan paniscus. To most biologists, these are distinct species. They certainly look and act differently. Bonobos are smaller, have different habits and their unique and promiscuous sex lives are legendar-y. Yet DNA tests reveal virtually no differences between the two "species". The case of the dusky seaside sparrow provides another interesting example. In 1987, the last dusky seaside sparrow, previously found all over Florida, died in captivity. its dark colour led taxonomists to define it as a subspecies, distinct from other seaside sparrows found along the Atlantic and Gulf coasts of North America. Despite the efforts of conservationists, the bird was wiped out along with its salt marsh habitat. Using some fancy genetic techniques, it was possible to extract DNA from preserved specimens and analyse it. Remarkably, this retrospective genetic study revealed that dusky seaside sparrows were genetically indistinguishable from Atlantic forms. Furthermore, the morphologically identical Gulf and Atlantic forms were genetically quite different from one another. The practical difficulties of using a single system for defining species make taxonomy a source of endless controversy. In general, taxonomists keep the BSC as an ideal concept, while taking into account morphological, ecological, behavioural and DNA differences as a measure of likely reproductive isolation. There are cases where all these measures tell the same story. Humans and chimpanzees, for example, do not breed, differ from one another in their morphology, and are on average about 1-3 per cent different in their DNA. In other cases, the stories are not the same. This tells us something about the complex processes that lead to speciation, the formation of new species, and the variety of means by which populations remain distinct in nature beyond simple reproductive incompatibility.
THE WORD "species" is actually Latin for "kind" or "form". Many alternatives have been suggested, and the list below outlines just a few of the more popular modern definitions.
Twist in the tale Darwin's finches
INTERESTINGLY, Darwin foresaw the problem of supposing that speciation was due solely to reproductive incompatibility. He rejected reproductive incompatibility as an absolute guide to whether two forms were distinct species because of inconsistencies between the degree of external difference between related forms and their interbreeding potential. All breeds of domestic dog, for example, can mate with one another to produce fertile offspring, despite the fact that they look remarkably different.
Figure 3: 21 x 21 grid map of Australia showing the species richness of eucalyptus trees (genus Monocalyptus). Darker squares indicate areas with more species within them
And as recent studies are increasingly showing, many apparently distinct species not only freely hybridise in nature but also remain distinct from one another. Darwin's finches were once cited as a classic example of how new species evolved, or "speciated", when geographically separated on islands. The 14 distinct "species" are all endemic to the Galapagos Islands, a volcanic archipelago lying a few hundred miles off the coast of Ecuador in the Pacific Ocean. Each species has a differently shaped beak, adapted for feeding on one type of seed. But here is the twist. Most people would think of Darwin's finches as "good" biological species. But recent studies show that some of these "species" freely interbreed in the wild to produce healthy hybrids. it is not clear why the groups remain distinct, but presumably hybrids with intermediate beak shapes are less well adapted for feeding, and lose out to the "pure" forms in the competition for food. When El Nifio triggered significant but temporary changes in the vegetation of the islands in the 1980s, the number of hybrids increased, and there are signs that differences between the forms are being further eroded. Darwin's finches are not an isolated example. Current estimates suggest that at least 10 per cent of animal species hybridise in nature. Birds, butterflies and coral reef fish all include huge numbers of hybridising species. These hybrids are not necessarily weak, sterile or deformed, but are frequently found to be healthy individuals capable of reproducing. Even the blue whale, the largest animal that has ever lived, has been found to breed in the wild with the fin whale, producing fertile offspring. In plants, hybridisation is so common that botanists have found the BSC practically unworkable.
Percentage of different bird groups hybridizing in the wild.
Conserving Species Think biodiversity
THE LESSON steadily emerging from such studies is that planning to preserve simply the maximum number of species is probably not the best approach to good conservation policy. Instead we must focus our efforts on preserving biodiversity-and conserve habitats with the broadest range of species or varieties. At present, it is usually the number of species in a particular habitat that is taken as a measure of the value of the environment in conservation terms. Governments or conservation groups confronted with the choice of preserving either habitat A or habitat B will usually count up the number of species in each habitat as the first step in their decision making. Using the BSC as the sole guide to con servation thinking has thrown up several anomalies. In 1973, the US Congress passed the Endangered Species Act (ESA), based on the BSC. But the weakness of this approach soon became apparent in 1977, when the Hybrid Policy dictated that hybrids between endangered species should not receive protection, because hybrids, it was argued, belonged to neither one parental species nor the other. The Hybrid Policy had further ramifica tions. There were suggestions that endan gered species which hybridised in nature should also have their protected status removed, because hybridisation meant that their genetic integrity - and hence their species status, had already been violated. There have been calls for the protected status of the threatened red wolf to be removed now that DNA tests have revealed that the wolves hybridised with coyotes at some stage in their recent evolutionary history. So far, these requests have not been implemented. As several biologists have pointed out, applying the BSC to the letter will leave few species on the endangered list, as it is probable that most species of an imals and plants have hybridised at some stage in the past. So instead of thinking only about species, biologists are now looking more at the raw material of species and sub species - the range of variation in their genes, morphology, behaviours and habi tats. Unfortunately, not even this approach gets us entirely out of the woods. The two populations of orangutans in Borneo and Sumatra are geographically separated, but virtually identical in physical characteris tics. However, they are distinguished by t slight differences in the sequence of their mitochondrial DNA. Some biologists 5 believe that these differences are sufficient for both populations to be afforded protected status. if the ranges of the two orangutan pop ulations ever merged, there is little doubt that they would form one reproductive group. But even avoiding the murky ques tion of whether or not the two populations are distinct species, we are left with the problem of whether each population des erves independently protected status based on a tiny difference in their DNA. If you look hard enough at two popu lations, you will almost inevitably find differences between them. Organisations such as the Natural History Museum, London, are now using the World Wide Web to advance new models for conserva tion decision making. These are based on the idea of preserving bio diversity-the diversity in genes, species and habitats. The new mod els suggest, for example, that con servationists should measure not only the number of species, but also how different they are. A habitat containing two closely related rare daisies would possibly rank lower than one containing a rare daisy and a rare orchid. The meaning of the term "species" has gone through many changes, driven on by new methods, the differing priorities of each scientific age and the varied fields of biological research. But all species definitions have been shown to have their limitations, and perhaps it is unrealistic to assume that we can impose and apply a single definition on a natural world made restless by evolutionary change. The natural world is an everchanging mosaic of form and function, with a staggering variety of morphological, behavioural, ecological and genetic differences. Perhaps biological and conservation thinking will, in the future, focus more on these differences, rather than the meaning and definition of one enigmatic word.
Martin Brookes is a science writer. All graphics are by Nigel Hawtin.