EVOLUTION IN ACTION: FROM MUSHROOMS TO TRUFFLES? PART 2

[Kendrick, B. 1994. Evolution in action: from mushrooms to truffles. II. McIlvainea 11 (2): 39-47.] [Continued from BEN 177]

In the first article, I described how various members of the mushroom genus Lactarius (family Russulaceae, order Agaricales) had evolved into rather strange forms. They had kept their distinctive microscopic characters: latex-producing cells which exude a unique milky fluid when broken; thin-walled, swollen sphaerocysts which make the tissues of the mushroom characteristically brittle; and a distinctive spore ornamentation of spines and ridges which often form a network, and which stain dark blue or almost black in iodine (what we call the amyloid, I+, or starch-like reaction). But the fruit bodies had taken on a distinctive appearance and also appeared to function rather differently.

In these evolutionary offshoots, three things have changed: (1) the peridium remains attached to the stipe at maturity, so the gills are not exposed to the outside atmosphere; (2) the gills are no longer plate-like, and are not oriented in a precise vertical plane; and (3) the spores are not forcibly discharged from the sterigmata. So despite having the characters listed earlier as being diagnostic of Lactarius, these forms are put in a separate genus, Arcangeliella, because the differences, especially the loss of the spore-shooting mechanism so characteristic of most basidiomycetes, are regarded as being of some basic biological importance. They affect the reproductive strategy of the organisms and therefore need to be taken account of when the taxonomy of the group is being established.

There are also even more reduced forms, in which the fruit body develops underground, the stipe is lost, and the gill tissues have become so folded and convoluted as to assume a spongy, chambered appearance: they are no longer gills, though they still bear basidia and produce basidiospores. So although these forms still have latex, sphaerocysts and amyloid spore ornamentation, they have been segregated in a third genus, Zelleromyces.

I concluded by saying that the Lactarius - Arcangeliella - Zelleromyces evolutionary pathway is not unique. In this second article, I will describe other similar developmental phenomena that have come to light, and the way in which they are now being interpreted.

The family Russulaceae, as understood by many mycologists, contains only two genera. We have already looked at one of them, Lactarius. Now let's consider the other one, Russula. This genus is very easy to recognize in the field, and (along with Lactarius) is one of the first genera the beginning amateur mycologist learns to identify. Russula has substantial fruit bodies, often with brightly coloured caps, stout stipes, and beautifully regular, white or cream-coloured gills. The caps, stipes and gills are brittle because their tissues contain clusters of round, thin-walled, turgid sphaerocysts. And the basidiospores have spiny, ridged and often net-like ornamentation that stains blue in iodine. Russula shares these two characters with Lactarius (which is why they are in the same family: these features are not found in any other agarics). But Russula has no laticiferous cells, and so does not produce latex (milk). This immediately distinguishes it from Lactarius, the milky cap, at least in most young, fresh collections.

Specimens are sometimes found which match the genus Russula in most ways, yet the peridium remains intact, attached to the stipe, and the gills are not exposed, even at maturity. In such specimens it will be seen that the hymenium has become highly convoluted or lacunose. Microscopic examination shows that sphaerocysts are present in the tissues, and the basidiospores do have blue-staining ornamentation; but although the attachment of the spores to the sterigmata is still somewhat asymmetrical or offset, those spores are not forcibly discharged. That is enough to exclude these specimens from Russula, and they have been placed in a separate genus, Macowanites.

Other atypical russuloid fungi have been found which resemble Macowanites in many ways: they still have sphaerocysts throughout the tissues, and spores with amyloid ornamentation. But they develop underground, and do not emerge, even at maturity. The external stipe has been lost, although a stipe remnant, in the form of a vertical column of sterile tissue, may still run through the fruit body. The spores, which are not forcibly liberated, are now symmetrically attached to their sterigmata. And the hymenium is no longer on recognizable gills, but lines convoluted or labyrinthine chambers. These specimens are segregated in the truffle-like genus Gymnomyces.

But this is not all. A second line of reduced forms appears to have originated from Russula. Some of these resemble Russula in many ways, having a stalk and a cap, sphaerocysts in the outer tissues and spores with amyloid ornamentation. But the gills have entirely lost their vertical orientation and perhaps even their integrity. The fruit body is now filled with a spongy mass in which the hymenium lines finely convoluted chambers whose walls lack sphaerocysts. And although the spores are asymmetrically mounted on the sterigmata, they are not discharged. This is the genus Elasmomyces.

Other specimens, while retaining sphaerocysts in their outer tissues and amyloid spore ornamentation, have retreated (or rather, remained) underground, have lost their stalk, and have become essentially truffle-like. Their internal arrangements are rather like those of Gymnomyces, but although they have sphaerocysts in their outer tissues, they have none in the walls of the hymenial chambers. These fungi are placed in the genus Martellia.

So, with a little imagination, we can visualize three lines of evolution, beginning with "normal" members of the family Russulaceae, mushrooms like Russula and Lactarius, and ending in truffle-like fungi which fruit underground.

Lactarius -> Arcangeliella -> Zelleromyces

Russula -> Macowanites -> Gymnomyces

Russula -> Elasmomyces -> Martellia.

Notice that the Russulaceae really contains not just two, but no fewer than eight genera, and that six of them, while microscopically "correct," do not give spore prints.

By now, you may suspect that there must be other such strange evolutionary pathways hiding among the rest of the agarics, and even in other groups of fungi. And your suspicion would be correct.

In fact, no fewer than 14 _ yes fourteen _ mushroom families have given rise to closed or underground forms which are treated as separate taxa. Let me sketch for you these lines of evolution as they are understood at present:

1. Russulaceae - see above

2. Cortinariaceae: the genus Cortinarius gets its name from the presence on the expanding basidioma of a special filamentous or cobwebby partial veil called a cortina (from the Italian for curtain). Many species also have brightly coloured caps. The basidiospores are rusty-brown in mass, and characteristically ornamented. Cortinarius has some species in which the partial veil does not open. But since the basidia still shoot their spores (they end up sitting on the inside of the veil), these species are retained in Cortinarius. In other Cortinarius-like specimens, the cap also remains closed, but careful examination shows that these have lost both the spore-shooting mechanism and the vertical plate-like organization of the gills: a section shows that the hymenium-bearing tissue has become convoluted and labyrinthine or spongy. These "aberrant" forms have been placed in the genus Thaxterogaster.

   Some species of Thaxterogaster seem to have lost their external stipe, but there is still a central column of white sterile tissue running up the middle of the fruit body. Other offshoots of Cortinarius have become entirely hypogeous, never emerging above the surface of the soil. These have lost all semblance of stipe and gills, look just like a truffle, and have been put in the genus Hymenogaster, although their basidiospores still closely resemble those of Cortinarius.

3. Agaricaceae: the genus Agaricus has given rise to sequestrate forms placed in the genera Endoptychum and Longula.

4. Lepiotaceae: Notholepiota is a sequestrate member of this family.

5. Amanitaceae: Torrendia is a sequestrate segregate of Amanita.

6. Bolbitiaceae: this family has given rise to a common and widespread sequestrate form called Gastrocybe. This is a strange fungus which appears in the grass during hot, humid weather. A narrowly conical, wet-looking brown cap arises on a long, narrow, delicate white stipe, which soon flops over. The spores sit squarely and persistently on the sterigmata. The whole cap soon dissolves into a slimy mass, which sticks to the grass. The spores never become airborne. We tend to assume that these spores are dispersed by grazing arthropods, although there is as yet no hard data to support that hypothesis.

7. Coprinaceae: Coprinus has given rise to a sequestrate form which is known as the desert shaggy mane. This fungus, which is put into the genus Podaxis, looks externally very like Coprinus comatus. Yet when a mature cap is cut open, the inside is seen to be filled, not with closely-packed, upwardly deliquescing gills, but with a dry mass of black spores, which will eventually blow away like dust when the outer skin of the fruit body erodes away or breaks. I have an excellent videotape sequence of this happening to a large specimen growing out of a termite mound in Africa (the Podaxis, unlike Termitomyces, apparently does not enjoy a mutualistically symbiotic relationship with the termites). The relationship of Podaxis with Coprinus is confirmed by the fact that under wet conditions, Podaxis, too, can undergo some deliquescence or self-digestion.

8. Strophariaceae: Stropharia is the presumed ancestor of the sequestrate genera Nivatogastrium and Weraroa.

9. Entolomataceae: Entoloma has spawned the sequestrate Richonia, the relationship being established by the pink colour and the distinctive angular shape of Richonia spores, which are almost identical to the spores of Entoloma itself. Nolanea may have given rise to Rhodogaster.

10. Tricholomataceae: Hydnangium appears to be a sequestrate derivative of Laccaria.

11. Gomphidiaceae: Gomphidius has hived off the sequestrate genus Gomphigaster, and Chroogomphus has produced Brauniellula.

12. Paxillaceae: Austrogaster and Gymnopaxillus are sequestrate derivatives.

13. Boletaceae: Boletus, Suillus and Leccinum have spawned above-ground sequestrate forms in Gastroboletus, Gastrosuillus and Gastroleccinum. Alpova, Truncocolumella and the extremely common Rhizopogon are below-ground, sequestrate derivatives of Suillus. The techniques of molecular biology have recently shown that, at least for certain parts of its genome, Rhizopogon is very closely related to the epigeous, spore-shooting Suillus (more closely, in fact, than Suillus is related to other genera of boletes).

14. Strobilomycetaceae: Gautieria is a fairly common hypogeous derivative, probably of Boletellus.

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