16 FUNGI Volume 2:3 Summer 2009

Species and Their Evolutionary Histories

Else C. VellingaDepartment of Plant and Microbial Biology, University of California – Berkeley

A M Y C O L E G I U M O F T H E L I T E R A T U R E

This anthology shines a spotlight on species. How are fungal speciescircumscribed, and how do we recognize them? How do we knowthat what we have now is the same as the original author had whenhe or she described the species a century ago? How are these spe-cies grouped by humans to reflect their evolutionary history?

In the spirit of Darwin, who was born 200 years ago andtraveled to uncharted territories and saw places where few hadbeen before, here, in our selection of articles on species and phy-logenies, we’ll opt for the lesser known journals, the roads lesstraveled, and those genera that do not normally bask in a sea ofattention.

This selection of recent articles is personal, hence biased,and there is no attempt to give a comprehensive overview of thehuge systematic and phylogenetic mycological literature.

Studies in Entoloma

Noordeloos, M.E., 2008. Entoloma in North America 2: the spe-cies described by C.H. Peck—type studies and comments.Österreichische Zeitschrift für Pilzkunde 17: 87–152.

Charles Horton Peck was a botanist in the state of New York from1867, and then the official state botanist from 1883 until his re-tirement in 1915. He described many new species of mushrooms;most of them came from New York, but he was in correspon-dence with people all over the country who sent him specimens.His descriptions, many of them published in the annual reports ofthe state botanist, are short, but typically include some informa-tion about the spores. Here is an example:

“Pileus thin, convex, glabrous, umbilicate, pale yellow, obscurely stri-ate when dry; lamellae thin, somewhat close, decurrent; stem slender, gla-brous, hollow, colored like the pileus or a little paler, commonly with whitemycelium at the base; spores subglobose, angular, 8–12 µ x 6-8 µ. Pileus2–2.5 cm. broad; stem 2.5–3.5 cm. long, 1.5–2 mm. thick.”

From these few lines of text, unaccompanied by photographsor drawings of the specimens, and lacking data on the rest of themicroscopic characters, it is hard to picture the species he had inhis hands. Fortunately, his collections were preserved and are inthe New York State Museum in Albany, NY. These collections canbe studied to reveal the secrets they have kept for over a century.

Furthermore, and this is most important, the whole myco-logical community profits when this research is done by a con-temporary who is knowledgeable on the group in question andcan place the species in a modern taxonomic context.

Machiel Noordeloos, the Dutch Entoloma specialist (Euro-pean authors recognize one big genus Entoloma; in the NorthAmerican tradition it is split up in a number of smaller generasuch as Alboleptonia, Leptonia, and Nolanea), has already studiedthe type collections made by Hesler, Alexander Smith, and Mazzer;now he has published his observations on Peck’s collections.

It is very helpful that he reproduces the original descrip-tions—albeit in a slightly different, but uniform format—and addsa wealth of microscopic characters, illustrated with line draw-ings. Most importantly, he gives extensive comments on wherethese species belong, and whether they might be the same as spe-cies described from Europe. The one big drawback is that thiswork is published in the journal of the Austrian Mycological Soci-ety; few people in America will think of looking for it there or beable to get a copy, short of contacting the author.

The description given above is that of Eccilia flavida, with aunique combination of characters within Entoloma: cylindricalcheilocystidia, a funnel-shaped yellowish pileus, and clamp con-nections at the base of the basidia. Its best fit could be (sub)genusOmphaliopsis.

The author can be reached at macrolepiota@comcast.net.

A Cortinarius species in sect. Calochroi, found in the Sierra Nevada, Cali-fornia, growing with pines, Douglas fir and red fir. This might be C.barbaricus, but a final identification awaits confirmation by sequencecomparisons. Photo by Dimitar Bojantchev, www.mushroomhobby.com.

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Cystoderma

Saar, I., K. Põldmaa, and U. Kõljalg, 2009. The phylogeny andtaxonomy of genera Cystoderma and Cystodermella (Agaricales)based on nuclear ITS and LSU sequences. Mycological Progress8: 59–73.

On account of its beautiful granulose covering and elegant ring,finding a Cystoderma is always a little thrill. However, that plea-sure is now a bit spoilt by the fact that the genus has been split intwo. One group has spores that stain grey to blue in an iodinesolution (“amyloid” in jargon), though this reaction may be lim-ited to a small part of the spore surface, and the other group doesnot show this reaction at all. The amyloid-spored group retainsthe genus name Cystoderma, and the other, less species-rich, groupis called Cystodermella. The two genera are both in the “Agaricoid”lineage, a group with predominantly dark spores, though the twogenera are not really close in evolutionary terms—their strikingcharacters having been invented twice. Cystoderma proper is posi-tioned close to Phaeolepiota aurea, which is also provided with agranulose covering, while Cystodermella is a sister to Ripartitella.The Estonian authors also focus on species delimitations, and in-clude many type collections in their study. Cystoderma fallax—awell known species in North America—shares molecular charac-ters with C. carcharias and is now considered a variety of that spe-cies. Several white species are either reduced to synonymy or low-ered in rank. Thus, Cystoderma niveum has become Cystoderma jasonisvar. niveum. In some cases, the authors are careful to maintain thetaxa already described, and recognize them now at variety level.One species, Cystoderma japonicum, is exceptional, as the sporesare not amyloid at all, and yet based on the shared molecular char-acters, it falls in the middle of Cystoderma. Unfortunately, whatother morphological characters might make it a real Cystodermaare not specified. The combination of phylogenetic analyses witha thorough nomenclatural overview of the species makes this papera valuable resource. In a separate paper, Vizzini (see below underStrophariaceae) has made several additional combinations, thoughwithout a thorough taxonomic treatment to back them up.

Climbing the mountain called Cortinarius, group by group

Dam, N., and Th.W. Kuyper, 2009. Het geslacht Cortinarius inNederland—IX. Groep 22: Telamonia’s met rood velum.Coolia 52: 87–111. [The genus Cortinarius in the Nether-lands—IX. Group 22: Telamonias with red veil.]

Garnica, S., M. Weiß, B. Oertel, J. Ammirati and F. Oberwinkler,2009. Phylogenetic relationships in Cortinarius, sectionCalochroi, inferred from nuclear DNA sequences. BMC Evo-lutionary Biology 9:1. (17 pp). www.biomedcentral.com/1471–2148.

I’d like to draw attention to an ongoing series of Dutch articles,the first appearing in 1998, in which the huge genus Cortinarius is

tackled group by group. These groups are circumscribed by simplefield characters that do not necessarily correspond to naturalgroups. Of course, the Netherlands is a small country, with a well-known and well-researched mycoflora, and in a continent with arich history of Cortinariology. Other places may not be so fortu-nate, but wherever you are, recognition starts with careful obser-vations, documentation, and the keeping of records. In the presentarticle, the authors display an intimate knowledge of every spe-cies and every collection ever made in the Netherlands, and la-ment the apparent rarity of species in this particular group.

This article, Number 9 in the series, treats the red-veiledspecies. That bit of red changes a dull dark-brown Telamonia intoan object of beauty and interest. The red color is caused by an-thraquinones, the pigments that make Dermocybes such won-derful dye mushrooms. When you are not sure whether the redon your veil is from anthraquinones or an other chemical, there isan easy way to tell: put a bit of the veil in water on a microscopeslide, put the slide under the microscope, from the side add 5%KOH, and pull it through with absorbent paper. Keep watching,and a miracle happens under your eyes when anthraquinones arepresent: the reddish veil exudes a pink-purple cloud, that shortlyloses all its color.

The second paper also treats one group within the big genusCortinarius, viz. section Calochroi—nice, colorful, big mushrooms.Here, however, a totally different approach is taken, and speciesfrom North America and from Europe are put in a single phylo-genetic context, based on DNA sequence data. What struck mewhen looking through this paper was that all the European spe-cies were named, whereas more than half of the species from NorthAmerica went nameless—there is still a lot to be done here, start-ing with describing, naming, and cataloguing!

Strophariaceae

Jacobsson, S. and E. Larsson, 2007. Hemistropharia, a new genusin the Agaricales. Mycotaxon 102: 235–40.

Redhead, S.A., J.-M. Moncalvo, R. Vilgalys, P.B. Matheny, L.Guzmán-Dávalos and G. Guzmán, 2007. (1757) Proposal toconserve the name Psilocybe (Basidiomycota) with a conservedtype. Taxon 56: 255–57.

Vizzini, A., 2008. Novitates. Miscellanea. Rivista di Micologia 51:63–66.

The genus name of Sulphur tufts was changed fromNaematoloma to Hypholoma so recently, that the need for furtherupheavals in the genus names for species in the Strophariaceaemay be rather upsetting.

Even before the molecular wave broke, there was already a lot ofdispute about how many genera there are in this family and howwe can recognize them. The main species were always easy to clas-sify, but borderline cases caused a lot of headaches, and their nam-

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ing history often showed a switch from one genus to another. Toput an end to these back-and-forth changes, some authors recog-nized only two genera: Pholiota for the brown-spored species, andPsilocybe for the rest, including Hypholoma and Stropharia.

Unfortunately, the DNA sequence data do not really supportsuch a simple world, and species from these genera end up scat-tered to different parts of the big tree, not nicely clustered asexpected from the morphological viewpoint. As soon as we beginto recognize smaller units as genera, many more demand to fol-low, and a process of balkanization grips the Strophariaceae. Onevictim of the new insights is the genus Psilocybe, in the old, narrowsense—but now it will be even more narrowly defined. Thereappear to be two groups, that are not closely related—one withspecies that contain psilocybin, and the other with those that donot. Of course, a little trap is set for us—the type of the genusPsilocybe is one of those little brown mushrooms, Ps. montana, with-out a bluing reaction. The name Psilocybe is so much associatedwith the hallucinogenic species that an official proposal to changethe type of the genus from Ps. montana to Ps. lanceolata has beenput forward. There is already a genus name available for the non-active species: Deconica, so that would be a perfect solution. Inthe process, a genus name will disappear: Melanotus is to be incor-porated with Deconica.

New genus names have been proposed for other members inthe family: for instance, Str. albocrenulata—one of those speciesthat was always difficult to place and had been classified variouslyas a Pholiota and as a Stropharia—now has found its true destina-tion in its very own genus, Hemistropharia. A similar fate befallsthe species usually known with the epithet “oedipus” under severalgenus names but, occasionally, known as “Phaeogalera dissimulans”:it, too, had wandered from one genus to another and now has itsown genus, Meottomyces. Meottomyces dissimulans is a rather non-descript brown mushroom with a hygrophanous viscid cap, palegrey-brown gills and a whitish stalk with a small ring;chrysocystidia, the cystidia with golden contents that are a char-acteristic of Pholiota species, are lacking, and the cheilocystidiaare plain.

Other unfamiliar genus names are Phaeonematoloma—a ge-nus that predates the molecular revolution—for the old Hypholomamyosotis, and Hemipholiota for the Pholiota species fruiting on cutsurfaces of poplar, Ph. populnea (synonym Pholiota destruens). Quiterecently, Leratiomyces was erected to contain Hypholoma aurantiacum(synonym Stropharia aurantiaca) and allies. Stropholoma had alreadybeen proposed for this group but, since the name was not pub-lished according to the rules of nomenclature, Leratiomyces takesover. Quite a mouthful for these ubiquitous wood-chip inhab-iters: Leratiomyces ceres (yes, the species name has also changed). Itis time for some immutable common names!

Brace yourself for more genus changes to come—Galerinaand Psathyrella are in line for a similar makeover.

Psathyrellaceae

Padamsee, M., P. B. Matheny, B. T. M. Dentinger, and D.J.McLaughlin, 2008. The mushroom family Psathyrellaceae: Evi-dence for large-scale polyphyly of the genus Psathyrella. Mo-lecular Phylogenetics and Evolution 46: 415–29.

Larsson, E., and L. Örstadius, 2008. Fourteen coprophilous spe-cies of Psathyrella identified in the Nordic countries using mor-phology and nuclear rDNA sequence data. Mycological Re-search 112: 1165–85.

Vašutová, M., V. Antonín and A. Urban, 2008. Phylogenetic stud-ies in Psathyrella focusing on sections Pennatae and Spadiceae—new evidence for the paraphyly of the genus. Mycological Re-search 112: 1153–64.

Nagy, L. G., S. Kocsubé, T. Papp, and C. Vágvölgyi, 2009. Phylog-eny and character evolution of the coprinoid genus Parasolaas inferred from LSU and ITS nrDNA sequence data. Persoonia22: 28–37. Open access at www.persoonia.org.

Psathyrellas are not the most visually appealing species; that maybe the reason that the many grey, brown, purple, cream specieswith pale to dark brown spores cry out to be classified. The clas-sic monograph by Alexander H. Smith (available through the NewYork Botanical Garden) describes many species, but neither placesthem in a phylogenetic context, nor makes it easy to identify them.

Some progress has recently been made by various researchgroups taking different approaches, namely tackling the genus ina wide context, examining only a few sections, or focusing on thedung-dwellers.

The first study tackles the whole family Psathyrellaceae, in-cluding the ink caps Coprinellus, Parasola, and Coprinopsis. By thetime these three genera were recognized as separate from Coprinusin the strict sense (shaggy mane, C. comatus, and C. sterquilinus, itssole surviving members, had been expelled to the Agaricaceae), itwas clear that their relationships with Psathyrella had to be re-examined. It now appears that the family Psathyrellaceae as a wholeis monophyletic (meaning that all its members share a most re-cent common ancestor and all descendents of this ancestor aremembers of the family), but that the genus concepts have to bereconsidered. Thirteen different groups have emerged; some con-sist only of species from one morphologically defined genus, butothers are a mixed bag. For instance, Psathyrella conopilus forms agroup together with Parasola species (ink caps with pleated caps,such as P. plicatilis) while some Psathyrella species, like Ps.marcescibilis, fall smack in the middle of Coprinopsis (the genus forC. atramentarius, C. lagopus, C. radiatus, C. friesii, C. narcoticus andmany others). Though this paper shows clearly that the old genusPsathyrella cannot be maintained in its present form, new generaor groupings are not proposed.

The second Swedish paper is one of those rare examples thatcombines descriptions with placement of all species in a phyloge-

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netic context using molecular data. In this case there are four-teen species, including two new ones. The ecology is covered aswell, and a key to the European dung-inhabiting species is given.

The third paper looks in detail at two sections, sectionSpadiceae in which the species have relatively small spores, andthick-walled cystidia, and section Pennatae, also with small spores,but with flask-shaped to wedge-shaped, often thick-walledpleurocystidia. A nice feature of this paper is that the morpho-logical characters are indicated in color on the phylogenetic tree.The general conclusions are the same as in the first paper:Psathyrella is a mess and needs to be sensibly split up, with somereshuffling of species.

The last paper focuses on Parasola, one of the offshoots of theold Coprinus, and a group that stands out in the field, as the caps ofthese species are indeed pleated like parasols. The emphasis hereis on species delimitation, using DNA sequence data, but again,with a sharp eye for morphological characters and how they changefrom one species to another. Despite extensive morphologicalwork on this group in Europe, some species still need more work.For instance, Parasola lilatincta is a name represented by two dif-ferent not closely related taxa, while some other species can nowbe merged: P. hemerobia with P. plicatilis and P. leiocephala with P.galericuliformis.

Xerula Down Under

Lebel, T., and P. S. Catcheside, 2009. The truffle genus Cribbea(Physalacriaceae, Agaricales). Australian Systematic Botany 22:39–55.

Petersen, R. H., 2008. The genus Xerula (Agaricales; Fungi) inAustralia and New Zealand. Nova Hedwigia 87: 1–67.

Some genera are just more appealing than others, and Xerulasscore high on my list of mushroom beauties—they are elegant,balanced, large enough in most cases to be spotted easily, andthey grow in nice places. These two papers treat the species fromAustralia and New Zealand—nice looking mushrooms with lotsof interesting characters. Petersen describes the species morpho-logically, and thoroughly. The other paper focuses on those spe-cies that do not actively discharge the spores, and whose gills arenot freely developed and remain enclosed (secotioid is the term).It actually came as a surprise to me, that Xerula has secotioid lin-eages. The phylogeny presented in this paper shows that thesesecotioid forms evolved several times, just as they did in Agaricus,Lactarius, Russula and many other genera. The spores of theseCribbea species are fantastic, with big wings or ridges. Until thephylogeny of the genera Xerula, Oudemansiella and Cribbea has beensorted out, these genus names will continue to be used. But, bewarned: right now it looks like Xerula is not monophyletic, andthat Oudemansiella and Cribbea form one lineage together with oneof the two Xerula groups.

Arctic MushroomsBaker Lake, Nunavut

gently nodding in the wind, they ask so little of this little-giving habitat . . . at leastthe morsel of it that wasn’t scraped away by Ice Age glaciers . . . they ask only forwater’s blessing on a sliver of soil or cushion of Cladonia lichen . . . and with thatblessing, a Cortinarius, Russula, or Lactarius will fruit here . . . then assume a magis-terial posture beside their ground-hugging neighbors . . . frailty, they seemto say, is in the eyes of the beholder . . . we are the mighty redwoods and giantsequoias of the tundra . . . abandon us not to your impatient boot . . . for our tawnyheads and moist bodies have a place in the world, too . . . we too owe our existenceto parental genes . . . the threads of our mycelia engage the ground no less firmlythan the stalks of your legs . . . it’s just that we travel down the river of time withslightly quicker paddle strokes than you . . . come back tomorrow, for instance, andwe’ll be gone . . . and all the more beautiful because of it

—Lawrence Millman