The Evolution of a Great-Big Headache:

"Understanding" Mushroom Taxonomy and Phylogeny

by Michael Kuo

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My Headache

My headache stems from the fact that I have just finished reading a little piece by Binder & Bresinsky (2002) telling me that DNA research reveals Gyroporus castaneus to be more closely related to Scleroderma citrinum than to Boletus edulis.

Hunh? I mean, really now! Look at these three mushrooms:

Gyroporus castaneus  Scleroderma citrinum  Boletus edulis

. . . and tell me you see what Binder & Bresinsky mean. A puffball and two boletes! Except that the bolete on the left is actually a kissing-cousin to the puffball in the middle, and not that genetically close to the other bolete. If mycology doesn't work out for them, maybe Binder & Bresinsky could guest on Sesame Street, bashing kids in the head when the poor fools think they've played "One of These Things Is Not Like the Others" successfully.

My headache aside, I am of course only joking about Binder & Bresinsky--and I do not doubt the validity of their findings. I understand so little of DNA science that I have no choice but to accept unconditionally what the experts hand down. Last month, I thought that DNA sequencing for mushrooms involved injecting rabbits with something from the mushroom and then sending something else that comes out of the rabbits to a big laboratory somewhere. I told all my friends. This month, reading different articles, the rabbits are gone. Binder & Bresinsky didn't use rabbits. I mention this rabbit-thing to emphasize my infantile understanding of molecular biology, but I promise I didn't make it up; see for example Jung et al. (1993), an experiment reaching important conclusions about morel taxonomy, in which methods included the following: "Rabbits were bled from their marginal ear vein [sic] to obtain preimmune sera"; and my personal favorite, "100µl of goat-antirabbit immunoglobulin antiserum coupled to horseradish peroxidase . . . were added to each well and incubated" (678).

Goat-antirabbit immunoglobulin antiserum?

My point is: What the hell is going on? Are we at the point where DNA research will re-align our groups of mushrooms in ways that make them seem to the naked eye (or even to the microscope) like alliances of strange bedfellows? What are we learning about the mushrooms themselves--how they evolved over time, how they function in ecosystems? What use can we make of our new knowledge?

We have not even come close to documenting all the mushroom species on the planet. Molecular biology represents at least the second (possibly the third or fourth) time the entire project has had to be reconsidered, and many backward steps taken along with the forward steps in order to account for previous "mistakes." The first time was caused by the microscope . . .

Mushroom Taxonomy by Morphology

Carl Linnaeus sensibly decided in 1735 that "objects are distinguished and known by classifying them methodically and giving them appropriate names" (19). So he proceded to do just that--for the rest of his life. If he could find it in nature, he named it. If his students could find it (he sent them packing all over the globe), they brought it back to him in Sweden and he named it. And he created an ingenious system for naming it, whatever it was: the familiar Genus species "binomial nomenclature" we still use today. He even named some mushrooms, and "L" for "Linnaeus" still hangs around, in the species-author gobbledygook that follows a mushroom's scientific name, for many species (Amanita muscaria, for example).

Linnaeus based his classification decisions on observation of details, and for him "the naming and ordering of the products of Creation linked the study of nature with the worship of God" (Farber, 11). The way to understand God was through an understanding of the perfection of His creation, and close inspection of the minutiae of species was the method for understanding. So Linnaeus arranged and re-arranged the species on earth throughout his life, attempting to understand the perfect system of God's creation, nature, by examining the features displayed in its parts . . . and therein lay the rub. Notice that, even as the cornerstones of modern taxonomy were being laid, one might have argued that what was being arranged was our perception of organisms, rather than the organisms themselves.

It was nearly a century later before Elias Fries (also a Swede; he even taught at the same university Linnaeus had) went the distance for mycology and published his Systema mycologicum (1821-1832), using Linnaeus's methods to classify what must have been just about every darned mushroom in Sweden. Anyone who has ever looked up mushrooms in books has seen the familiar "Fr." following many species names. Like Linnaeus, Fries worked without the benefit of a compound microscope [ ¹ ], so his classifications were based on observation of the mushrooms' macrofeatures--including a new emphasis on the color of the spore print. Mycologists still refer to the mushrooms he classified this way as being defined in "the Friesian sense," or as "Friesian species."

Over the course of the 19th Century, mushroom taxonomy advanced many long strides as "natural historians" across the globe followed the road mapped out by Fries. Natural history became a public fascination (see Farber, 2000) as museums in Europe and North America displayed exotic animal and plant species from all over the world in intriguiging "dioramas" and proudly featured reconstructed dinosaur skeletons. Popular "botanical gardens" sprung up in major cities, visited by hundreds of thousands of people. John Audubon is a good example of the kind of naturalist doing 19th-century "field work" in what we now call biology. His beautiful paintings of North American birds are well known; he traveled across the continent searching for all the birds he could find--and, after briefly observing their habits, shot them. He frequently shot over 100 birds a day--but was careful to illustrate them soon after death, before their colors faded (Farber 31-32, 51).

It was in the context of the cultural "event" of natural history that much of mushroom taxonomy advanced. Collecting specimens from nature and classifying them became a Victorian fascination, and members of the leisure class and academia named many new mushroom species and erected many new genera to put them in. Popular mushroom "field guides" were published, often with an eye towards edibility. A look at the list of previous publications in W. H. Gibson's Our edible toadstools and mushrooms (1895) gives one a sense of the 19th-century naturalist mindset:

The Works of W H Gibson

Actual professional mushroom specialists were few and far between--and most of these were employed by botanical gardens or as "state botanists." In many ways, Charles Peck (1833-1917) exemplifies mycology at the turn of the century. As botanist for the New York State Museum Peck described over 2,700 mushrooms, publishing his findings in the "Annual Report of the State Botanist" (Haines).

Peck's compound microscope gave him magnification of about 500x. This enabled him to discover many things about the mushrooms he found. He observed spores, gill faces, and other mushroom tissues. Here is a more or less typical example of Peck's mushroom descriptions, for Boletus illudens, a species he authored in 1897:

Pileus convex, dry, subglabrous, yellowish brown or grayish brown, sometimes tinged with red especially in the center, flesh pallid or yellowish; tubes bright yellow, plane or somewhat convex when old, adnate, their mouths angular to subrotund, often larger near the stem; stem nearly equal, sometimes abruptly pointed at the base, glabrous, pallid or yellowish, coarsely reticulated either wholly or at the top only; spores oblong or subfusiform, yellowish-brown tinged with green, .00045 - .0005 in. long, .00016 - .0002 in. broad.

Pileus 1.5-3 in. broad; stem 1.5-2.5 in. long, 3 to 5 lines thick.

(Quoted in Smith & Thiers, 1971; 243)

What I find interesting about Peck's descriptions is that they are more or less parallel to descriptions used in today's field guides, more than a century later. Careful observation of a mushroom's macrofeatures, combined occasionally with rudimentary microscopic observations like spore size and shape, still form the basis for identification for many mushroomers (and mycologists); this site's identification strategies, for example, are essentially the strategies of Peck--and our species page for Boletus illudens includes little information beyond what Peck observed, other than the fact that the cap flashes green with ammonia.

Even at 500x, however, microscopes like Peck's began to reveal curious things. Peck's contemporary William Murrill (1869-1957), for example, published a treatment of North American boletes in the first-ever edition of Mycologia (1909), in which the following couplet was included:

    Spores brownish-black, rough, subglobose . . . . . . . . . . . . . . . . . . . . . . . . . Strobilomyces

    Spores ochraceous to yellowish-brown, smooth, usually oblong-ellipsoid . . . . [continue]

    (The Boletaceae of North America, p. 4)

Not that the spores of Strobilomyces species were particularly useful as a way to distinguish them from other boletes (anyone who has ever seen the Old Man of the Woods knows there are plenty of macrofeatures to do this job), but Murrill did notice that the species in Strobilomyces had round, reticulate ("rough," to his microscope) spores. (For light microscope and electron microscope images of the spores of Strobilomyces confusus, see its species page at Halling & Mueller's Macrofungi of Costa Rica.)

Mushroom Taxonomy by Microscopy

The example of Strobilomyces represents an instance in which what was discovered under the microscope more or less confirmed a classification already made on the basis of macrofeatures--like the darker spore print, also mentioned in Murrill's couplet. It was not long, however, before microscopic examination began to reveal differences that were not paralleled by differences in macrofeatures--and all hell broke loose.

As the 20th Century progressed, mycologists like C. H. Kauffman (1869-1931), Alexander H. Smith (1904-1986), and Rolf Singer (1906-1994), to mention only a few of the North American "giants," used better and better microscopes, and began to reclassify mushrooms on the basis of what they were seeing under the lens. Smith's 1947 monograph of Mycena in North America, for example, separated 232 species into subgenera and sections, in a key based extensively on microscopic features. Introducing this mammoth treatment, Smith wrote:

    At the present time generic concepts in the gill fungi may be said to be in a state of transition. The genera of the Friesian classification have been critically evaluated in the light of information obtained on microscopic characters and as a result of the discovery of many interesting species from other parts of the world, and it has become evident that considerable regrouping throughout the agarics is desirable.

    (Preface, vii)

Though Smith was discussing gilled mushrooms, I will use boletes to demonstrate the kind of "regrouping" he mentions as resulting from microscopic examination; the same "state of transition" certainly manifested itself with boletes as well. And, anyway, I have been using boletes as examples so far--and it was a bolete postulated as a puffball relative that caused the headache that caused this essay in the first place! Consider these two boletes:

Boletellus pseudochrysenteroides  Boletus rubellus
Click images to enlarge.

At the macrofeature level there is little, if anything, to indicate that one of these two mushrooms does not belong in the genus Boletus. Anyone who has flipped through a field guide looking at pictures of boletes knows how widely variable in appearance species of Boletus can be--but in the case of these two mushrooms, there are not a lot of macrofeatures separating them even as species. But look at the spores of two mushrooms under the microscope . . .

Boletellus pseudochrysenteroides spores  Boletus rubellus spores

. . . and they are clearly distinct. The mushroom on the right (in both pairs of illustrations) has typical Boletus spores--elliptical and smooth. The mushroom on the left, however, has spores that are elliptical, and roughly the same size--but are longitudinally ribbed in a way that is noticeable even with my amateurish microscope and camera techniques. Only a handful of boletes, out of hundreds in North America, have spores like this. For this reason they are placed together in the genus Boletellus, which includes the mushroom on the left, Boletellus pseudochrysenteroides. The mushroom on the right belongs in Boletus, as one would have expected by looking at its macrofeatures; it is Boletus rubellus.

Smith & Thiers defined Boletellus in 1971 like this: "The spores are furnished with more or less longitudinal wings, ridges, or striations," adding that "[i]n most other respects the species are quite diverse" (381). Pinning a genus entirely on microscopic features, while admitting that the included species are macroscopically divergent (take a look at Boletellus russellii and Boletellus ananas) takes a bold step away from Friesian taxonomy.

The separation of Boletellus on the basis of its ornamented spores seems to make sense--unless you think about the fact that little or nothing has actually been theorized about the mushrooms to justify splitting them off. In other words, when we say that new equipment or technology has enabled us to see physical differences that were hidden before, we may be saying more about the technology than about the mushrooms--especially if we remain mute when it comes to attempting to explain why, for example, the mushrooms in Boletellus developed ribbed spores. I will return to this issue later; for now I simply want to point out that microscope-based taxonomy proceded rather uncritically and without much self-reflection as it became popular in the 20th Century--just as Linnaeus, 200 years earlier, did not bother to theorize why the things he observed were like they were, since they were representatives of God's perfect creation.

The Golden Age of the microscope in North American mushroom taxonomy (and we are definitely still within it) is epitomized by the works of Smith and L. R. Hesler. Aside from using powerful microscopes to analyze and measure spores, Hesler & Smith studied the cellular ("hyphal" in the fungus world) structures of mushrooms, and focused (oops) on differences they discovered. In 1963 they arranged the waxy caps into subgenera and sections based entirely on the arrangement of cells in the gills ("intricately interwoven," "somewhat interwoven," "divergent," and so on). Interestingly, however, the subsequent arrangement of subsections, "series," and species for the 244 mushrooms is accomplished primarily on the basis of old-fashioned, Friesian macrofeatures. Hesler & Smith's 1979 treatment of Lactarius is also an interesting combination of macroscopic and microscopic emphases; see their Key to Subgenus Lactifluus, Section Lactifluus for a brief example.

Hesler & Smith collected a stunning number of North American mushrooms, and authored many species. But each time Alexander Smith sat down to arrange a genus of mushrooms, with or without a collaborator, he was obliged to re-study the collections of earlier mycologists, such as Peck, under the microscope. In short, all the data compiled before the emphasis on microscopic features must be re-examined. This project--re-evaluating mushroom taxonomy in light of the microscope--is far from over, despite the prolific contributions of Smith and many others, which is why I said we are still in the microscope's Golden Age.

Mushroom Taxonomy by Molecular Biology

Simultaneously, however, new taxonomic tools have not only knocked on the door but have been making themselves at home for a number of years. Analysis of the chemicals present in mushrooms has led to questions that Friesian and microscope-based taxonomy may be unable to answer. Additionally, laboratory experiments performed on mushrooms in culture (like, petri-dish culture; not social culture) are producing interesting results, some of which may challenge our taxonomical assumptions. But the biggest and loudest stranger suddenly getting comfortable on the couch is the molecular biology person--the one who coolly bandies phrases like "goat-antirabbit immunoglobulin antiserum." As I hope I made clear above, this stuff gives me a headache. Whereas I can get out my microscope and see the spores of Boletellus pseudochrysenteroides for myself, I can't exactly pull out my DNA sequencing stuff, or my RFLP equipment (don't ask) and fire it up. All I can do is ask molecular biologists to tell me what they have learned about mushrooms by torturing rabbits.

I can approximate an answer on when moleculary biology stuck its foot in the door, however. A quick trip through the citations in the extensive entry for "Molecular Biology" in Ainsworth & Bisby's Dictionary of the Fungi (Kirk et al., 2001) makes it clear that DNA studies on fungi got into full swing in the early 1990's (327). To double-check, and to stick to the bolete theme of this essay, I searched "boletus" in the CABI Bioscience Bibliography of Systematic Mycology, which returned the titles, authors, and dates of some 600 publications related to Boletus, stretching back about 20 years. The earliest bolete publication I can find that is clearly (to me, anyway) based on DNA science is from 1990.

So for about 10 or 15 years molecular studies have been performed on mushrooms, perhaps rather haphazardly; which mushrooms get studied is more or less a matter of chance. I have been told that molecular research is probably more reliable when it comes to separating large groups of mushrooms--"clades," in molecular parlance--and less relevant (though not irrelevant) when it comes to separating species. This may be due in part to the fact that mushrooms simply have "less DNA" than humans, for example, giving scientists fewer data to work with. Regardless, however, the technology is still in its infancy, and this limitation may disappear with advances in equipment, software, and the like.

It goes without saying that the project of using molecular studies to review the mushroom taxonomy already accomplished on the bases of macrofeatures and microscopes has barely begun. One step forward; two steps back.

Why Phylogeny Was Ancillary to Mushroom Mycology until Recently

It isn't easy to find sources, written prior to the molecular biology era, on the evolution of mushrooms . . . and that in itself tells you something. What seem to me to be the most important questions--things like "What survival advantage caused the selection for ribbed spores in Boletellus?"--were until recently frequently treated as afterthoughts by the science of mycology. It is as though the mammoth project of simply cataloging mushroom species (and reorganizing the species already cataloged) so occupied everyone's time that the science wound up neck-deep in a can't-see-the-forest-for-the-trees scenario.

But you can hardly blame the mycologists. Above, I described three enormous taxonomic projects, and briefly alluded to two others (biochemistry work and studies in culture). If the first project, cataloging the morphology of mushrooms, is something like half-way done (two-thirds?), the second, based in microscopy, might have managed to reconsider 70-80 percent of that effort. The other projects have just begun. As an amateur mushroomer, when I collect a mushroom, bring it home, describe its macrofeatures thoroughly in my journal, illustrate it with scans or photos, preserve it, and later look at its spores and tissues under the microscope, I have already spent at least two or three hours with the mushroom. Then there is the time it takes to sift through the literature to identify it--which can take a few minutes or many hours. I'm not even counting the travel time for collecting or the time it takes to write about the mushroom if I create what is, by mycological standards, a very simple species page for this Web site.

Mycologists, of course, are better at these things than I am, and the process is sometimes more streamlined and efficient for them. In fact they are not even obligated to collect their own mushrooms; for an account of the process by which new species get collected by mushroom clubs on "forays" and turned over to mycologists who have agreed to serve as temporary experts or to lecture on mushrooms (and an interesting portrait of the social and political dimensions of this arrangement), see Fine (1998, 221-247). Professional studiers of mushrooms also have access to one another's collections, and the collections of mycologists through history (Peck's collections, for example, are still available). But since thorough study of as many collections of a mushroom as possible is required before a mycologist can stake her reputation on published claims about the species, it's clear that studying mushrooms collected by others adds to the amount of time rather than reducing it.

In light of this assessment of how much time it takes to study a mushroom and publish your findings, recall the work of Alexander Smith. The Mycena monograph treats 232 species; Hygrophorus treats 244; Lactarius treats 200; Boletes of Michigan treats 213. Other Smith publications include treatments of Leucopaxillus, Tricholomopsis, Cystoderma, Naematoloma, Psathyrella, Pholiota, Crepidotus, Phaeocollybia, Heboloma, and Puffballs and Their Allies in Michigan. The typical "Material Cited" list in the description for just one of the thousands of species represented by Smith's work includes a dozen or so collections, many of them made by Smith himself. Shakespeare wrote 37 plays, five long poems, and 100 14-line sonnets. Some literary scholars believe this output could not have been generated by one person, and in my field there is a debate about how many Shakespeares there really were. If there weren't so many people around who knew Alexander Smith and worked with him, historians of mycology might do the same thing for "Alexander H. Smith"!

There aren't very many mycologists in the world--and these days the vast majority of them study things besides mushrooms. There is no "Department of Mycology" in any American university (Fine, 1998, 222), and schools like the University of Illinois, formerly prestigious in mushroom studies, stopped renewing the mushroom chairs years ago as more and more resources were devoted to the big funders of agribusiness and the healthcare industry. Even within the depleted ranks of mycologists, "those who study the taxonomy of large fleshy fungi . . . have particularly low standing, and jobs for their students at major teaching institutions are rare" (Fine, 222). So the task of merely cataloging the earth's mushrooms, even if all of the actors were as prolific as Smith (they aren't), is frankly impossible. Not enough people, not enough time. Add to this the sisyphean element discussed above (the taxonomy technology boulder falls back on mycology every time it gets rolled part-way up the hill) and it seems clear to me that if mushroom science had waited for the catalog to be finished before theorizing about evolution, the theorizing wouldn't have happened.

The Linnaean Rut

The study of mushrooms got stuck in a non-theoretical rut right at the beginning, I believe, simply because it developed as a Linnaean effort. Linnaeus, recall, strove to discover the system of nature, God's perfect creation. "God has suffered [me] to peek into his secret cabinet" (Hagberg, 208), Linnaeus wrote. Since creation is divine, it is perfect--and therefore static, unchanging, immutable. We now know, of course, that nature is not static (and in the realm of theology, we also know that believing in nature's constant evolvution is not irreconcilable with belief in God). But the funny thing is, people knew this in Linnaeus's time, too. Darwin's 1859 Origin of Species did not introduce the idea that there were forces in nature that changed it, acting according to laws we could discover; this was a contribution of the Enlightenment, occurring everywhere around Linnaeus, who scorned any secular science.

In France, for example, Linnaeus's contemporary Buffon spent his life writing the 36 volumes of Histoire Naturelle ("Natural History"), treating all living things--and minerals--on earth. The difference between Linnaeus and Buffon is evident even in the titles of their life-works; Linnaeus sought to discover the system of nature (Systema naturae), while Buffon wanted to tell its history. Buffon's project is a narrative, while Linnaeus's is a catalog.

    Buffon sought to supply his generation with a total picture of nature. He did so in a new fashion: historically. To understand the present, according to Buffon, one had to know the past. If a set of internal molding forces interacted with the environment over time, the key to explaining present-day living forms lay in uncovering the history of life on Earth.

    (Farber, 2000, 20)

If the classification of mushrooms had been picked up by figures sympathetic to Buffon (and later Darwin), rather than (philosophical) odd-balls and reactionaries like Fries and Peck, modern mushroom taxonomists might have inherited a system that strove to discover how mushrooms evolved, and strove to explore variation rather than stasis.

Accounts of Elias Fries tend to mention his eager devotion to Goethe's German Romanticism and its "idealistic morphology" in passing--as though the belief that ideal, archetypal biological forms manifested themselves in the earth's many organisms would not come to bear in important ways on his taxonomy. Fries was warned by his teachers not to attend the university in Uppsala, where Naturphilosophie reigned supreme, so he studied in Lund instead. Somehow, however, Goethe's ideas crept into his life, and by the time he published the first volume of the Systema he was a convert. Soon thereafter he was teaching at Uppsala (Ainsby, 259-261; Backlund, 2000).

Fast-forward to 1979, and we can see an unfortunate result of Fries's romanticism:

    This variant, common in southeastern Michigan, has "passed," in North America, as a pale Lactarius insulus. The concept of the latter, as represented by the accounts of Burlingham (1908) and Kauffman (1918), calls for a species with coppery orange conspicuous zonations. This concept is clearly out of line with the description of L. insulus by Fries (1821). . . Since the 1821 description is the one that validates the species, we believe that a type should be selected to conform to it, in which case L. zonarius might fall into synonymy with L. insulus. This is a problem for consideration among the European mycologists who, we hope, will engage in the establishment of types for these species.
    Hesler & Smith (1979, 269-270)

Here Hesler & Smith discuss a "variant" of Lactarius psammicola, agonizing over the lack of established "types" for several European species, including one named by Fries. Type species are selected representatives for mushroom species, collected by an authority, described thoroughly, and preserved (or at least photographed) for future reference. Now, things are more complicated than I am allowing here; modern biologists follow rules established by various international conventions convened over the years to sort out differences in names and approaches. But it is not entirely coincidental that Fries believed Lactarius insulus to be an ideal form, manifestations of which he collected in Sweden in the early 19th Century--while Hesler & Smith, inheriting Fries's taxonomical tradition, examine mushrooms collected over 100 years later and thousands of miles away and still wonder whether their specimens match an ideal, static "type."

It was in Fries's lifetime that Darwin's Origin was published, but by all accounts his reception of Darwin was one of skepticism. By the end of his life he had lost interest in his life's passion, in part due to his dissatisfaction with the rising hegemony of microscope work.

Peck was a devout Presbyterian who did not curse, smoke, or drink, and who "believed in a simple, straightforward world governed by the Creator. His was a world where species did not change. His views against Darwin were firm" (Haines, 1998). A refusal to accept Darwin at the turn of the century is frankly reactionary. Historians of science have amply demonstrated that, while Darwin's ideas provoked (and still provoke) substantial outrage in the general public, the scientific community of his time accepted the basic premises of his theory within a few years of the 1859 publication of Origin:

    [B]y the late nineteenth century . . . Darwin had convinced the scientific world that evolution of living forms had occurred and that change in time explained many of the central issues of natural history. The disagreements over the factors in evolution encouraged research along many different pathways. Comparative anatomy continued to be a major tool of investigation, but new and exciting lines of research soon developed.
    (Farber, 2000, 70-71)

Despite Peck's substantial and significant contributions to the study of mushrooms, one cannot excuse the fact that, as a 20th-century scientist, his theory explaining the development and function of Boletus illudens was: "And God said, Let the earth bring forth grass, the herb yielding seed, and the fruit tree yielding fruit after its kind, whose seed is in itself, upon the earth: and it was so." But does Peck's reactionary position come to bear on his contribution to mushroom taxonomy? Not according to modern mushroom scientists, to judge from the parenthetical way they treat Peck's anti-Darwinism, Linnaeus's refusual accept the Enlightenment idea that species changed over time, or Fries's devotion to idealistic morphology.

Missing Data

It seems clear to me that Peck's reactionary position did influence modern mushroom taxonomy, as did the world-views of Linnaeus and Fries, if for no other reason than that these perspectives allowed mushroom taxonomy to develop in what is essentially a theoretical vaccuum. Genesis is a theory, but it is not a particularly good one, when rendered by fundamentalists.

To see how a static view of nature would affect mushroom taxonomy, imagine for a moment that you are Charles Peck, hunting mushrooms in New York on a sunny afternoon. You come across a mushroom you have collected many times. It takes you only a few seconds to figure this out--and since you are not collecting edibles today, you move on. Soon you come to a mushroom that inspection reveals is one you may not have seen before. Here is one of God's creations that you have not yet encountered. Because of your experience with collecting and describing mushrooms, you know that you should carefully collect as many specimens as you can, in all stages of development. You search around until you can find no more specimens, then return to the laboratory with your basket.

Back at the lab, you carefully record all the mushroom's details, paying attention to a series of features long established to help separate species. You make a few notes, then carefully preserve the specimens. Later--perhaps much later--you research all the known mushrooms (a process considerably expedited by your experience) and find that your mushrooms do not answer the descriptions of any similar mushrooms, in Europe or North America. You are used to this happening; most of your sources are European, and not much work has been done on American taxa. Eventually you decide that you have discovered a new species, and publish your description so that others will be able to refer to it.

Now recast the story so that you are a different Charles Peck. You can curse, smoke, and drink--or not; we'll leave that part up to you. But let's assume you have read Darwin and you are excited by the idea that species evolve over time. You see the woods as an amazing and beautiful battleground where species compete to survive. You often recall Darwin's work with barnacles, in which he studied 10,000 examples and was able to arrange many of them in serial progressions demonstrating gradual changes in their features. In short, your concept of "species" involves not earthly, individual manifestations of a divine plan, but rather the idea of evolving populations.

What would you do differently as this imagined Charles Peck? In an effort to see evolutionary patterns, you might pay more attention to similarities between mushrooms, rather than ignoring them to focus on differences. You might not have skipped over the mushrooms you recognized so quickly, because careful attention to their features might help establish a "range" of possibilities within the species. More importantly, though, you might collect much more--and very different--data than the real Peck did. You would certainly describe the mushrooms carefully, but you might also have taken the time, in the woods, to carefully note many details about where and how the mushrooms were growing: the trees they were associated with, details about the habitat like moisture content, elevation, wind exposure, the age of the forest . . . in short, everything you could think of that might come to bear on an explanation for the mushrooms' selection for survival.

Darwin would never have reached the conclusions he reached about species on the Galapogos Islands if he had not observed them interacting with their environments. It is only very recently that what we now call "ecological studies" have been done on mushrooms. For more than 200 years, mushroom taxonomy progressed without the collection of much of the data needed for evolutionary analysis--despite the fact that scientists in other fields collected it regularly.

Pattern Recognition as Phylogeny

Another set of missing data that has hampered efforts to theorize the evolution of mushrooms results from the lack of a decent fossil record. Mushrooms, as any collector knows, are ephemeral, which makes them unlikely candidates for fossilization. This is not to say that we have discovered no fossils, but the few discoveries made have as yet done relatively little to inform our ideas about the evolution of mushrooms. So, until recently, we were left nothing to base our phylogenetic proposals on, other than a large catalog of mushroom descriptions in the Linnaean tradition, and a fairly large number of preserved specimens in herbaria. Under such conditions, little could be done beyond what I would call simple "pattern recognition"--an inductive process generating a picture of evolution by careful speculation about the features of existing mushrooms.

Here is an example--or, rather, a section of an example, again using Peck's Boletus illudens. Consider the question of how the pores of this mushroom evolved. One theory, based on intuitive speculation, might be that the pores were at one time gills. The so-called "gilled bolete," Phylloporus rhodoxanthus, might occur to us as a crucial mushroom to include in such a speculation, since so many of its macrofeatures (and its microfeatures) parallel those of the boletes. It looks like a bolete, but it has thick gills that run down the stem. It also might occur to us that the various "boletinoid" boletes--some species of Suillus, for example, or Gyrodon merulioides--might be seen as transitional, since the pore surface tends to run down the stem and often approximates gill-like structures, especially near the stem. Thus we might compose a progression like this:

Progression to Boletus illudens

. . . from the gilled bolete, to boletinoid mushrooms like Suillus umbonatus, to mushrooms like Boletus illudens. We might even theorize that the vaguely reticulate stem apex in Boletus illudens represents a remnant of the previous condition.

The problem is, while such speculations are attractive and often convincing, they are only fantasy--no matter how clever they are--without the support of ecological evidence (the "missing data" I discussed above) or other kinds of support that I will discuss shortly. And, speculative progressions based on intuitive readings of macrofeatures do not actully constitute theories; they are merely arrangements of taxa based on appearance. When Darwin arranged barnacles or birds he did so on the basis of their appearance and careful study of what the changes in macrofeatures--beaks, for example--accomplished for the species. The progression above, by contrast, does not even consider the question of what is accomplished for Boletus illudens by a selection in favor of its pore surface.

Modifications to the Column

At some point in the last half of the 20th Century, or maybe in the last quarter of it, an actual theory began to be developed about the evolution of mushrooms, which I will call the Column Modifications theory. I am only half kidding when I say it might have been sheer embarrassment that prompted mycologists to come up with something besides clever portraits of patterns in macrofeatures. Other sciences--admittedly, with the benefit of substantial fossil records and geological evidence--had managed to produce many phylogenetic theories. In fact several theories from other disciplines came to bear on mushrooms, especially the "discovery" of Pangaea (the world's former supercontinent, now fractured) and the theories about forest evolution emerging from the field of paleobotany.

Since so many mushrooms are involved in associations with trees ("mycorrhizal" relationships, in mycologese), and since paleobotany was beginning to produce a convincing history of the way trees evolved (see Miller & Watling, 1987), it made sense to theorize a concurrent evolution for mushrooms. What was missing was a notion of what selective forces might operate on mushrooms to cause changes in their morphology. The answer that gradually emerged was: "spores, spores, spores." There is a sense in which the spores of a mushroom are like its children. So few of them will survive (by winding up in a favorable substrate and germinating), that a mushroom must do everything it can to hedge the odds. Thus, two primary selection pressures were determined:

  • Protect spores until they are mature.
  • Increase the area of the spore-bearing surface and adjust its position, to facilitate greater dispersal of more spores.

Here, at long last, we have an actual theory. Miller & Watling's 1987 "Whence Cometh the Agarics? A Reappraisal" puts the various pieces of the theoretical puzzle together for the Basidiomycetes, serving as a sort of "Modern Synthesis" for mycology (albeit 40 or 50 years late) by combining the insights from geology and paleobotany with the observations of mycology--the information on morphology and microfeatures from the Linnaean catalog, of course, but also the emerging studies in culture and in biochemistry. According to the Column Modifications theory, a simple spore-bearing column "arose," probably prior to 300 million years ago, lifting its spore-bearing surface above the forest floor to catch air currents above the litter. The early, simple column would have corresponded to modern "earth fingers" like those in the genus Clavaria. The two selection pressures above operated over the millenia, resulting in the development of a cap (partial protection for the spore-bearing surface) and, later, the development of gills and pores, which rather ingeniously increase the area of the spore-bearing surface.

By way of a quick analogy, imagine lightly gluing seeds to a sheet of cardboard, then going outside to wave it in the air so the seeds will fall. Other arrangements, however, would increase the number of seeds you could disperse. You could take a larger sheet of cardboard and fold it, like a corrugated roof, so that the total surface area for gluing seeds was greater, but you could still easily manage to hold it. This development, according to the Column Modifications theory, corresponds to the chanterelles with their folded undersurfaces, protected by a rudimentary cap. Eventually you might arrange other systems that would hold even more spores. If you were to take many sheets of cardboard and affix them at right angles to your original sheet, leaving a small space between the hanging sheets, you would approximate gills, which dramatically increase the surface area. Pores, in this analogy, might correspond to a strategy in which you affixed many cardboard tubes (paper-towel tubes, for example) at right angles to the original sheet of cardboard, after gluing the seeds to their interior surfaces.

In the gilled mushrooms, selection pressure to protect immature spores then resulted in modifications to the cap shape and, eventually, to the development of protective membranes to cover the spore-bearing surface until maturation. The pinnacle of this evolution is represented by a mushroom like Amanita muscaria, which has many gills that are lifted high above the forest floor, but protected in early stages of development by a partial veil and a universal veil.

Here, then, is a visual representation of one branch in the Column Modifications theory, leading to Amanita muscaria:

Evolutionary Progression to Amanitaceae

From top: Clavulinopsis laeticolor, Clariadelphus pistillaris, Cantharellus lateritius, Hygrocybe conica, Entoloma salmoneum, Laccaria laccata, Pluteus cervinus, Amanita muscaria var. formosa.

PK: Pamela Kaminski; GB: George Barron; CR: C Ribet; MK: Michael Kuo; JC: Jim Croce.

The series represented by this graphic is enormously appealing and seems attractively logical; as Miller & Watling put it, "[i]ts beauty is its intrinsic simplicity, and the ease by which a column of tissue can be formed with an amphigenous hymenium producing sexual spores" (445). But I hasten to add several things. First, that discoveries from molecular biology and elsewhere may or may not confirm the Column Modifications theory--or they may do so in some areas of the tree, and not in others. The boletes, for example, are less clearly arranged on the tree. Miller & Watling place them on a branch that tentatively arises from the coral mushrooms and moves through gomphoid mushrooms like Gomphus floccosus to the Paxillaceae (mushrooms like Paxillus atrotomentosus), then to the boletes. But if you recall the "headache" that began this essay, something is obviously missing from this portrait--namely, funky tough-shelled puffballs.

I should also point out that I manipulated the image above to make it more clever. The second stage, represented by Clariadelphus pistillaris, is my own insertion; it is a "simple column" mushroom that appears to be a mid-point in the development of the cap later accomplished by the chanterelles. Additionally, I selected mushrooms with similar colors to make the progression more appealing visually, and I paid careful attention to layout and orientation, arranging the mushrooms to emphasize the overall line created by the graphic.

At the base of the evolutionary tree proposed by Miller & Watling is a division between Clavaria-like mushrooms and Ramaria-like mushrooms; the Clavaria line leads through the chanterelles to the Amanitaceae and the Tricholomataceae, while the Ramaria line leads through Gomphus-like mushrooms and then splits into three lines, with one headed through Gymnopilus to mushrooms like those in Agaricus and Coprinus, another through the Dermocybe section of Cortinarius to the Cortinariaceae, and a third headed through Paxillus to the boletes, discussed above. The basal division generating these lines, mushroom collectors might have noticed, is spore color; the first line contains white- and pale-spored mushrooms, while the other lines contain dark-spored mushrooms.

It would be nice if the entire tree did not grow from an untheorized split on the basis of macrofeatures, but I do not find the theory. Instead, Miller & Watling write:

    In an earlier Symposium of this Society, in 1979, Watling (unpublished) offered a scheme of interrelationships between the families of agarics . . . suggesting an early separation of two main streams of agarics; one pale or white-spored agarics and another coloured spored, the former evolving from the latter by simplication of the spore-wall, a phenomenon seen even in present-day taxa.

What is lacking here (though for all we know it may be included in the unpublished manuscript) is a theory of what selection pressure would cause the "simplification of the spore wall" in the first place, resulting in a split between pale-spored and dark-spored mushrooms. Whether or not this apparent oversight has implications for the evolutionary tree constructed over it is beyond my ability to determine--but at least one recent molecular study has put white, brown, and black-spored mushrooms in the same phylogenic "clade" (see Johnson & Vilgalys, 1998, discussed below). [ ² ]

The Neolecta Effect-a

One problem with the Column Modifications phylogeny involves a bias towards the construction of a progression, from simple to complex, "primitive" to "advanced." Now, it may well turn out to be the case that the Column Modifications theory is supported, and that such a progression did in fact occur. But it is worth noting that evolution, as it is currently understood after the so-called "Modern Synthesis," does not progress according to a plan, and is not directed towards an anticipated end-point. Nature is replete with examples of evolution towards simplification, rather than complication, of forms. The fact that amanitas like Amanita muscaria have throughout human history received so much attention, and even been revered by many cultures (including the Romans), may or may not have anything to do with the generation of a theory that places them at the top of evolutionary achievement. But we should bear the potential bias in mind.

If we turn to the Asomycetes, we find that relatively recent discoveries have, in fact, revealed such a bias in the Column Modifications theory. Miller & Watling conclude their 1979 argument on the Basidiomycetes with a reference to the ascos: "It is by modification of this column that the agarics, polypores and hydnums have developed in a parallel way to the morels from the ascomycetous disc" (445). The parallel Column Modifications line for the ascos might look something like this:

Progression to Morchella esculenta

From top: Otidea onotica, Rutstroemia luteovirescens, Cordyceps ophioglossoides, Microglossum rufum, Leotia lubrica, Morchella semilibera, Morchella esculenta.

RN: Richard Nadon; MK: Michael Kuo

This is completely my construction, so don't blame Miller & Watling. I took their disc-to-morel proposition and filled in what seem to be reasonable steps. The simple, spore-bearing surface of the disc is raised, then raised higher to facilitate spore dispersal. The cup shape is revised, since it is inefficient, and becomes a multi-sided surface capable of catching air currents from all sides. The spore-bearing surface is then modified, one step at a time, to the large surface area of the yellow morel, which is pitted and ridged to increase spore holding capacity even more. Steps between the "jelly babies" (Leotia lubrica) and the half-free morel (Morchella semilibera) might even be added, going through Gyromitra and/or Helvella.

For a brief diversion, notice how the Column Modifications theory here appears to give credence to the "ontogeny recapitulates phylogeny" idea, first asserted by embryologists like Haeckel at the turn of the century. The idea is that an organism repeats, in its individual development, the pattern of evolution expressed by its species over time. Thus the embryos of fish, turtles, and man are strikingly similar--and the human embryo, for example, progresses through stages remarkably similar to the "lower" organisms. A developing morel is not an embryo, but take a look at its early stages:

Development of Morchella esculenta Ascocarp
Development of a yellow morel (
Morchella esulenta)

Photos © 1982. The New York Botanical Garden. [ ³ ]

As far as I can see, however, there is really not a whole lot to be done with the idea that ontology recapitulates phylogeny, other than to notice the striking coincidence when it occurs, and, as MushroomExpert.Com contributor Robert Zordani suggests, put a big "That's Nice" next to it. If the idea could be used to predict (post-dict?) earlier forms, its power would increase, but I doubt this is the case.

In fact, with the ascos anyway, mycology is now fairly sure that the development of an individual morel does not parallel the evolution of ascomycetous mushrooms; nor does the emerging picture of ascomycete evolution fit the Column Modifications theory particularly well. Much to the surprise of everyone, the genus Neolecta has been revealed as "basal" in ascomycete evolution.

Now, the Ascomycetes include many mushrooms familiar to mushroomers, like the morels, false morels, many cup fungi--and so on. But the ascos also include yeasts, molds, and a whole host of stuff that mushroomers usually pay no attention to unless they need penicillin to treat an infection. In fact all of this "weird stuff" comprises the bulk of the Ascomycetes; what we call "mushrooms" are in the minority. The genus Neolecta is in this minority, and it is represented by only three species: Neolecta vitellina, Neolecta flavovirescens, and Neolecta irregularis, which looks like this:

Neolecta irregularis
Neolecta irregularis

Recent molecular biology studies tell us that Neolecta was around in the lower Devonian period, about 400 million years ago! Today's three species "may not look like dinosaurs but could, in fact, be seen as living fungal relics of the past" (Landvik et al., 2001, 1151). This revelation has stunned the mycological world, because it raises the possibility that the unicellular yeasts derived from the filamentous Neolecta.

The "bias" I mentioned above, the fact that the Column Modifications theory loads a notion of progress into its operating system, may be starkly revealed after the Neolecta discovery. It may be possible to salvage part of the Column Modifications picture of the ascos, but other parts approach the nonsensical:

Speculation: The Neolecta Effect-a on Column Modifications

From top left to bottom right: Neolecta irregularis, Saccharomyces cereviseae yeast growing on pizza; Cordyceps ophioglossoides, Rutstroemia luteovirescens, Otidea onotica; Leotea lubrica, Morchella semilibera, Morchella esculenta.

RN: Richard Nadon; GB: George Barron; MK: Michael Kuo.

Again, this graphic is my creation, so don't blame the mycologists. About the only branch that makes any sense under Column Modifications is the branch leading to the yellow morel. The middle branch, headed for the cup fungi, reverses what seemed like fairly good logic, so that the mushrooms decrease the ability of the spore-bearing surface to catch wind currents, and descend to the forest floor, rather than arise from it. The top branch, in which Neolecta somehow heads for the unicellular yeasts, defies common sense.

Yet this is what molecular biology is suggesting may be the case. To be honest, I would imagine that much (if not most) of the picture of mushroom phylogeny is still so out of focus that graphics like the ones above will eventually turn out to be theoretical relics in a debate that eventually provides a much clearer--and probably very different--picture. But I am thankful that the debate has begun; mushroom science went for hundreds of years without even asking the questions! This is an interesting and exciting time to be a mushroomer, as research from many areas (several of which I have left out of this discussion entirely) is conducted and the long, dialectical process of arguing over results begins.

Headache Postponed

If you are still reading, I thank you for your patience!

My headache, caused by the revelation from molecular biology that one bolete was more closely related to a puffball than to most other boletes, is gone--gone because, since its onset, I have spent days and days with my nose buried in mycological texts, and had the choice of letting it get worse, or getting over it. So, just as the dense mass inside Scleroderma citrinum turns to spore-dust and winds up being shot into the air when raindrops fall on the puffball, my headache disintegrated and blew away. It is not worth having a headache over these issues when so little is known and so much remains to be seen.

Over the past fifteen years or so, insights into mushroom phylogeny from molecular biology have snowballed. Now mycology journals are full of papers investigating the big questions. With a little research, in fact, it became evident to me that Binder & Bresinsky's research was not even the first to suggest the relationship between Scleroderma and Gyroporus. Molecular biology has quite simply stood Friesian taxonomy on its head. As Hibbett and Donoghue (1998) put it:

    The central goal of taxonomic mycology is to create classifications that communicate understanding of fungal phylogeny. . . The current taxonomic system, which is based on the hierarchy of Linnaean ranks and the International Code of Botanical Nomenclature, is unsatisfactory for this purpose.

A few months after Hibbett & Donoghue's assessment that Linnaean taxonomy might be doomed in the fungal world, for example, Johnson & Vilgalys (1998) published a paper in the same journal after submitting a number of gilled mushrooms to DNA research. They found, among other things, that Coprinus comatus, the Shaggy Mane, may belong in what used to be called the Lepiotaceae, along with the Meadow Mushroom, Agaricus campestris. With this, we're talking white-spored, brown-spored, and black-spored mushrooms in the same groups! They also found that some of the satellite genera created over the years out of Lepiota--like Chlorophyllum and Leucoagaricus--may not be supported by molecular evidence (splitters will be happy to know that Leucocoprinus, at least, was tentatively supported).

This is a bad time to demand answers from mushroom mycology, or to insist on a stable picture. But it may well have been this insistence on a stable system--a Linnaean, or Friesian system--that led mushroom science to the uncomfortable position of sitting in the 21st Century with few answers, a crumbling taxonomy, and a lot of work to do. Amateur mushroomers, too, have a lot of work to do, if they're interested. No, we cannot extract DNA or conduct mating research in petri dishes. But we can definitely help provide missing data to the specialists, who need information on the distribution of species, and as much ecological data as can be gathered. Our collections are important, especially when illustrated, described, and preserved. Those of us who have been collecting mushrooms more or less the way Peck did, a hundred years ago, should consider changing our habits so that we gather ecological data as well--not just the mushrooms.

Boletus parasiticus
Click to enlarge.

One last question: What are they going to do with Boletus parasiticus? If you are not familiar with the mushroom, it is a small bolete that parasitizes the puffball Scleroderma citrinum, growing right out of its body! Where does this little guy fit into the picture?


¹  Fries seems to have distrusted microscopes, as did Linnaeus. Microscopic structures in fungi had been discovered even in Linnaeus's time, and by the Friesian era, Schaeefer, Persoon, and Léveillé had even gone so far as to observe and illustrate spores, basidia, sterigmata, and cystidia on gill faces. These discoveries did not begin to impact mushroom taxonomy, however, until later. See Ainsworth (1976). [ return to text ].

²  One complication I do not explore here involves the various "secotoid" and "gastroid" mushrooms--the funky ones rarely encountered by most mushroomers (I've never seen one) that have collapsed caps and infertile, malformed spore-bearing surfaces inside; many of these mushrooms apparently even grow more or less underground. They are attractive to scientists arranging phylogenetic sequences, however, since they often appear transitional. Some of them are included in the Binder & Bresinsky study. See also Thiers (1984). [ return to text ].

³  Reprinted with permission from The New York Botanical Garden Press. Originally published in R. Ower, Notes on the development of the morel ascocarp: Morchella esculenta. Mycologia, Vol. 74, pp. 142-144, figs. 2, 3, 4 & 5, copyright 1982, The New York Botanical Garden. [ return to text ].


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Cite this page as:

Kuo, M. (2003, February). The evolution of a great-big headache: "Understanding" mushroom taxonomy and phylogeny. Retrieved from theMushroomExpert.Com Web site:

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