BEN # 178

Adolf Ceska aceska at CUE.BC.CA
Wed Nov 26 02:32:06 EST 1997

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No. 178                              November 25, 1997

aceska at        Victoria, B.C.
 Dr. A. Ceska, P.O.Box 8546, Victoria, B.C. Canada V8W 3S2

From: Dr. Bryce Kendrick <mycolog at>

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

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 characteris-
tically 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

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,  espe-
cially  the loss of the spore-shooting mechanism so characteris-
tic 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 ornamen-
tation, they  have  been  segregated  in  a  third  genus,  Zel-

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

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 Lac-
tarius) 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  ornamenta-
tion  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  asymmetri-
cally  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

So,  with  a little imagination, we can visualize three lines of
evolution, beginning with "normal" members of  the  family  Rus-
sulaceae,  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 microscopi-
cally "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

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  se-
questrate forms placed in the genera Endoptychum and Longula.

   (4) Lepiotaceae: Notholepiota is a sequestrate member of this

   (5)  Amanitaceae:  Torrendia  is  a  sequestrate segregate of

   (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,  nar-
row, 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  deli-
quescing  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 se-
quence 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  relation-
ship  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 se-
questrate 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.

[Continuation in BEN # 179]

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