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Authors: Richard Fortey

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The author handles an edible black true truffle (
Tuber
) from Sardinia.

Evidence from molecules was quite quickly incorporated into the intellectual armoury of the more forward-thinking systematists. For a while there was resistance in some quarters by experts who trusted implicitly their traditional characteristics for classification—colour, or hairs on legs, or behavioural patterns—and did not like the suggestions of new evolutionary relationships thrown up by molecular studies; and it was also true that in the early days some dubious conclusions were drawn from using the wrong “designer gene” for a particular job. However, it was soon recognized that sequencing evidence could provide answers to questions that had been troubling systematists for years. I will give just one example. Edible truffles are subterranean fungi, belonging to the genus
Tuber.
There are several species, and gourmets dispute their relative merits.
Tuber magnatum,
the white truffle, which grows in Italy, commands the highest prices—up to about $5,000 a kilogram. It is the most expensive foodstuff in the world. The Périgord truffle,
T. melanospermum,
is mostly French in origin, and black rather than white. The warty summer truffle,
T. aestivum,
grows in England, but is less sought after, although it is the only one I have found in the wild. All are remarkable for having an extraordinary, and some would say irresistible, odour, which suggests a kind of mushroom/meat hybrid. This intense fragrance is imparted to oil or eggs, and indeed the simplest way to eat truffles is to use them to flavour an omelette, or to grate them finely over scrambled eggs.
Pâté de fois truffé
is such stuff as gourmet dreams are made of. The edible properties of the truffle are not matched by their aesthetic ones, for most truffles look like some kind of knobbly animal excreta which have been passed with not a little discomfort. They do not have to impress with their appearance, for it is the smell that matters. In the wild they grow close to the roots of trees, particularly oak (
Quercus
) and hazel (
Corylus
); they are one of a very large number of fungi that form a symbiotic relationship with the tree host, their mycelium enveloping or penetrating the roots in a so-called mycorrhiza. The host benefits from ions such as phosphate that the fungus can “hunt” from the surrounding soil, while the fungus receives products of photosynthesis from its tree host in return. The problem for the fungus is how to spread its spores from underground and hence ensure its survival, and this is where the smell comes in. The spores are enclosed in chambers or fissures inside the truffle. Animals such as wild pigs find the smell of the truffle attractive, and will greedily grub up the fruit bodies. “Truffle pigs” are trained to smell out the subterranean booty, which is removed from them before they can gobble it up. But when ingested, the spores will eventually pass out of the animal, unharmed, in droppings, having by then been dispersed widely from their point of origin. In rainforests in south-eastern Australia I have seen holes scratched by marsupial potoroos in search of truffles—very different creatures performing the same favour for a truffle on the other side of the world.

When the truffles were first recognized as fungi rather than some spontaneously generated freak of nature, it was thought that such curious productions comprised a single group of organisms—a reasonable assumption, one might think. They deserved one of Linnaeus’ high-level classification tags—an Order. But when microscopes came to be focussed on the tissues inside the truffle, where the spores were developing, an interesting discovery was made. Not all truffles were alike. Those that graced the tables of the rich and hedonistic showed features at the microscopic level like those of another gourmet treat, the morel (
Morchella esculenta
). In other, and more technical, words they were ascomycetes. These fungi bear their spores inside minute sacs or asci of the order of a tenth of a millimetre long—there are usually eight such spores, so the asci have a very typical microscopic appearance, rather like eggs wrapped in a sausage. However, some other truffles, for example a genus called
Hysterangium,
showed evidence that they were related instead to the gasteromycetes—the group of fungi that includes puffballs and stinkhorns. These are basidiomycetes, which carry their spores in an entirely different way from the ascomycetes; they are typically borne atop a special cell called a basidium, usually four spores in a loose cluster. The white mushrooms that fill vats in supermarkets are distantly related basidiomycetes, as are the majority of fungi that troop through the woods in autumn. The ascomycetes separated from the basidiomycetes very early in earth history, and certainly more than a billion years ago. It is preposterous to classify truffles together that have such different evolutionary origins—and so the ascus-bearing truffles were separated from the basidium-bearing truffles: so far, so sensible, and resulting in two Orders. For common names we now had “truffles” and “false truffles.”

However, the story did not end there. From other microscopic hints there were suspicions that there were several origins for truffles in
both
the ascomycete group and the basidiomycete group. Truffles might have arisen repeatedly, on separate evolutionary trees, for all their superficial similarity. The closest relatives of a truffle might prove to be one of several different kinds of more normal-looking mushrooms and other fungi. The truffle shape, including its subterranean growth, is a specific adaptation—a mode of life, if you like. It was not so difficult to imagine a “truffle habit” originating several times, because most fungi do indeed develop underground, and only later erupt at the surface. If development were somehow “arrested” at the early stage—well, then you might have something like a truffle. The trouble is, how could you pair the truffle with its closest-related mushroom, since there is so little general resemblance between them? This is where the molecular evidence should come into its own. The appropriate mushroom partner should, in principle, show more similar sequence patterns at the molecular level to its truffle relatives than it does to other truffles or indeed other mushrooms. So it has proved. Using the appropriate genomic tool, especially one known as ribosomal ITS (Internal Transcribed Spacer), the complexity of the origin of truffles has been demonstrated. It turns out that at least six different kinds of mushrooms—that is, the basidium-bearing kind—have become “truffleized,” to coin a term. To add to this there are several more origins of truffles of the ascus-bearing kind, of which the true truffle,
Tuber,
is one. Far from being a natural group of organisms, the truffles originated from numerous different fungi on several different occasions, and it all probably happened millions of years ago.

Why should anyone care about such apparently esoteric information? After all, most people can happily pass their lives without seeing a truffle of any kind, and who but an outstanding eccentric would spend hours carefully digging around in the litter under trees to find false truffles of the inedible kind? But then, who would guess that truffle evolution was crucial to the survival of several charming Australian marsupials? For the Australian group of truffles, including some placed in the genus
Hydnangium,
were also independently evolved in close association with
Eucalyptus
trees. These false truffles provide a prime foodstuff for bettongs and potoroos, which are delightful, nocturnal cat-sized animals that are now the focus of intensive conservation efforts. The more that is known of their requirements, the more likely they are to survive in the twenty-first century. False truffles are as important to their continued existence as keeping them from the depredations of feral cats. So what might at first seem extraordinarily specialized information has links to those “pretty furry things” after all; nature is seamless, its connections multifarious.

The truffle example also links back to where we started—the questions of taxonomy. Every time a truffle under examination turns out to be related to an entirely different mushroom, we can imagine a curator cursing quietly under his breath and moving the relevant preserved specimens to a different drawer. This is an extreme case of “revision”—revisiting taxonomy. The point is that we expect classification systems, genera, families and so on in ascending order, to reflect fundamental resemblances between the species included in them. The species themselves are the units of this classification—at least they are if we have recognized them correctly—and they are the real things that get shifted around from one drawer to another. The genus or family whose name might be written on the drawer or cupboard is a
theoretical
concept, subject to change as science advances. As with the truffles, species may be added or taken away or moved around. The up-to-date taxonomist wants his classification concepts to square with modern views. For most such scientists this means that the species included in a genus, for example, should have descended from a common ancestor—that is, constitute what is known as a
clade.
The characters shared by the species in a genus—and nowadays these can be molecular characters as much as the traditional “hairs on legs”—are what define it, make it a natural entity. Discover new characters and the concept of the genus may well change, and so will the species included within it. This results in changes in generic names for a given species that irritate many people, and particularly knowledgeable amateur scientists. “Why do they have to keep changing the names?” is a common complaint. However, the contemporary investigator is obliged to seek out genera, or families, that are clades; the scientific method used in recognizing these groups is known as cladistics; and the whole business of examining relationships between organisms in this way is usually termed phylogenetic analysis, or simply phylogenetics. If names have to change as a result of careful reconsideration of species, well, that’s the price of progress. Much modern taxonomy is based upon computer analysis of relationships, where all the characters possessed by a group of organisms under study are allowed to fight it out until the “best” arrangement of species is discovered, resulting in a diagram—a cladogram—showing how species relate to one another. The eventual classification is then drawn up directly from the cladogram. For example, several clades of species clustering together might be recognized as separate genera, and if these genera then cluster together in a more inclusive group this larger group might be the basis of a family.

This sounds technical, and so it is. Quite a few famous taxonomists are computer experts first, and lovers of organisms second. They think in algorithms rather than algae. They are mostly interested in animals and plants as experimental material for their classificatory computer programs. Their conversation tends to revolve around the statistical criteria for the support of one piece of the cladogram or another; an outsider hearing these people chatting might think she was overhearing an unknown Amazonian language. However, arcane though it might sound, the cladistic approach has made taxonomy much more of a science, and less dependent on the word of an authority alone. It provides a unifying method across the spectrum of organisms, from virus to vicuña, and can embrace all kinds of evidence, from the molecular to the anatomy of a blue whale. But it will be clear by now that it also makes problems for that Linnaean system of naming animals and plants. Linnaeus himself designed his “system of nature” before the notion of evolution had gained currency. Some might have considered that the order of nature might be an expression of the mind of God alone: “he made them high and lowly, he ordered their estate,” as the hymn puts it. The idea that classification might involve notions of descent from a common ancestor was a subsequent introduction. The species as the unit of currency of classification was the only thing in common between these pre-and post-Darwinian worlds. And with the arrival of cladistics and molecular analysis the old Linnaean system might be seen to creak and groan under the stress of frequent changes in nomenclature—so much so that some scientists have tried to persuade their colleagues that the time has come to abandon the Linnaean binomial altogether. They want to replace it, or at least augment it, with something called the PhyloCode.

As this is written, the PhyloCode is still undergoing its own evolution, and it might be premature to anticipate the outcome. Many critiques of the Linnaean system are surely correct. There is no consistency in the use of the ranks of the system between different kinds of organism; some parts of the natural world have small genera, other parts have large ones, and a family can be a very different concept from one worker to another. We already have an intuitive feel for this. Birds are finely divided into genera separated by tiny anatomical differences; on the other hand, some genera of plants and fungi might include several hundred species. The attractive sea snail genus
Conus
includes at least six hundred species. The recognition of what makes a genus or family is partly a matter of tradition and taste. It is also undoubtedly true that there are not enough categories to recognize all the different levels of relatedness that a modern cladistic “phylogenetic tree” can recognize, and nobody wants extra formal ranks with names like supersubfamilies or subsuperfamilies. There are quite enough names already.

PhyloCode is based entirely on cladistic phylogenies, and provides a system for naming clades—all of them. The old formal Linnaean categories above species level are abandoned. This is a rather revolutionary suggestion, to say the least, and it is not surprising that it has excited some strong opposition. To my mind the strict logic of the PhyloCode is beside the point. The most important thing about the current system of naming organisms is the common language it provides, not just to other systematists, but to the rest of the world—people like gardeners, or bird watchers, or fungus forayers. Very few members of this larger community know about the details of cladistic phylogenetic analysis, and I suspect that most of them want a meaningful label that they understand rather than reassurance that every category is quite the latest collection of good clades. The 250-year tradition since the great Swedish systematist does count for something. Many of the common categories that a naturalist will comfortably recognize are old Linnaean families. Think of lilies (Family Lilaceae) or daisies (Family Asteraceae) or crows (Family Corvidae). These turn out to be pretty good clades as well, meaning that the resemblance between the species in the families does indeed reflect descent from a common ancestor. In my experience more “difficult” groups of organisms are often reanalysed time and again using the latest cladistic bells and whistles or new molecular evidence, and each new analysis is rather different from the last one. Nor is there any guarantee that the latest version is always the best. Potentially all these different analyses could be named under PhyloCode. In my view this would allow for just too many valid names, as each successive analyst sought to put his imprimatur on his briefly dominant hierarchy. But most important of all is a feeling that offends my democratic instincts, in that the systematization of nature would be even more in the hands of a coterie of specialists sitting in front of their computers than it is now. The binomial system has faults, but I suspect any new system would develop as many. The naming process would be taken away from the naturalists, nature lovers and intelligent laymen, at a time when there has never been so much pressure on the survival of species, or, indeed, on the survival of the taxonomists who know about fleas and carabids, trilobites and ammonites, grasses and orchids, or deep-sea worms. It is the survival of the biological world and of the basis of expertise that studies it that is the real concern of the twenty-first century. Names are the least of it.

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