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doi: 10.1098/rspb.2004.2759
, 1777-1782271 2004 Proc. R. Soc. Lond. B
A. B. Munkacsi, J. J. Pan, P. Villesen, U. G. Mueller, M. Blackwell and D. J. McLaughlin
growing ants−mushrooms by fungus
Convergent coevolution in the domestication of coral
References
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Received 14 February 2004
Accepted 25 March 2004
Published online 21 July 2004
Convergent coevolution in the domestication of coral
mushrooms by fungus-growing ants
A. B. Munkacsi
1
,J.J.Pan
2
, P. Villesen
3,4
, U. G. Mueller
3
, M. Blackwell
5
and D. J. McLaughlin
1
1
Department of Plant Biology, and
2
Department of Ecology, Evolution and Behavior, University of Minnesota,
St Paul, MN 55108, USA
3
Section of Integrative Biology, University of Texas at Austin, Austin, TX 78712, USA
4
Bioinformatics Research Centre, The University of Aarhus, DK-8000 Aarhus C, Denmark
5
Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA
Comparisons of phylogenetic patterns between coevolving symbionts can reveal rich details about the evol-
utionary history of symbioses. The ancient symbiosis between fungus-growing ants, their fungal cultivars,
antibiotic-producing bacteria and cultivar-infecting parasites is dominated by a pattern of parallel coevolu-
tion, where the symbionts of each functional group are members of monophyletic groups. However, there is
one outstanding exception in the fungus-growing ant system, the unidentified cultivar grown only by ants in
the Apterostigma pilosum group. We classify this cultivar in the coral-mushroom family Pterulaceae using
phylogenetic reconstructions based on broad taxon sampling, including the first mushroom collected from
the garden of an ant species in the A. pilosum group. The domestication of the pterulaceous cultivar is inde-
pendent from the domestication of the gilled mushrooms cultivated by all other fungus-growing ants. Yet it
has the same overall assemblage of coevolved ant–cultivar–parasite–bacterium interactions as the other ant-
grown fungal cultivars. This indicates a pattern of convergent coevolution in the fungus-growing ant system,
where symbionts with both similar and very different evolutionary histories converge to functionally ident-
ical interactions.
Keywords: convergent coevolution; symbiosis; fungus-growing ants; species assembly; phylogeny
1. INTRODUCTION
Phylogenetic approaches are commonly used to elucidate
the various dynamics of coevolutionary interactions
(reviewed in Page 2003). Phylogenies of symbionts have
been compared to infer the processes that underlie coevolu-
tionary interactions. Many coevolutionary interactions
exist between monophyletic groups of symbionts, such as
the gopher–gopher lice, beetle–ambrosia fungi and fig–fig
wasp systems (Hafner & Nadler 1988; Farrell et al. 2001;
Cook & Rasplus 2003), suggesting a single origin for these
interactions. These systems are examples of parallel co-
evolution, where functionally equivalent interactions exist
between specific clades of symbionts. However, the
assembly of functionally equivalent interactions is not lim-
ited to parallel coevolution; in rare instances, one or more
of the symbionts within a functional group can come from
distantly related clades. We refer to such phylogenetic
incongruence, i.e. polyphyletic origins of symbionts in a
functional group, within systems dominated by parallel
coevolution as convergent coevolution. By identifying and
determining the phylogenetic position of a poorly studied
fungal cultivar, we show that there is convergent coevolu-
tion in the fungus-growing ant system.
The ancient quadripartite symbiosis between fungus-
growing ants, their fungal cultivars, the fungal parasites
that infect the fungal cultivars and the bacteria used by the
ants to control the growth of the parasites is a model
example of coevolution (Currie et al. 1999, 2003; Mueller
2002). The ants eat the fungi as their main food source,
while the fungi benefit through propagation by the ants.
Ants inoculate new gardens with fungi from older gardens,
such that specific fungal cultivars are passed from garden to
garden within an ant lineage. Nearly pure cultures of veg-
etative mycelia are maintained with the help of antibiotic-
producing bacteria, which inhibit the growth of fungal
parasites that infect the fungal cultivars (Currie et al. 1999).
Four main lineages of fungal cultivars are grown by the
210 species of fungus-growing ant. Three out of the four
main cultivar lineages have the same ancient evolutionary
history as the ants that grow them and the parasites that
infect the cultivars (Currie et al. 2003). The fourth cultivar,
grown only by ants in the Apterostigma pilosum group, has
not been identified, but it has been predicted to have an
evolutionary history that is distinct from those of the other
cultivars (Chapela et al. 1994; Currie et al. 2003). To deter-
mine the pattern of coevolution of the A. pilosum cultivar
and its symbionts and to study the fungus-growing ant sys-
tem as a whole, the identity and origin of the cultivar grown
by the A. pilosum group must first be known.
The identification of the four main lineages of fungal cul-
tivars has been hindered by the absence of taxonomically
informative morphological characters in the nest mycelium
and the inhibition of mushroom production by the ants.
Phylogenetic analyses of vegetative mycelia (Chapela et al.
1994; Mueller et al. 1998; Johnson 1999) and identifi-
cation of ant-garden-borne white-spored gilled mushrooms
(reviewed in Muller 2002) led to the classification of three
Author for correspondence (munk0009@tc.umn.edu).
Proc. R. Soc. Lond. B (2004) 271, 1777–1782 1777
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2004 The Royal Society
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fungal-cultivar lineages in the family Lepiotaceae. Twelve
out of the thirteen genera of fungus-growing ants grow one
of the three lepiotaceous cultivars.
Previous phylogenetic analyses have suggested that the
fourth cultivar, grown by the A. pilosum group, was also
domesticated from a gilled mushroom (Chapela et al. 1994;
Villesen et al. 2004). However, mushroom production in
nature or in the laboratory has never been reported for this
cultivar. In this study, we use phylogenetic analyses to
identify the A. pilosum cultivar. We show that it is phylo-
genetically and morphologically distinct from the other cul-
tivars and discuss how this cultivar converged to the same
coevolutionary interactions as the other cultivars, despite
its distinct origin.
2. MATERIAL AND METHODS
(a) Isolation and voucher of specimens
Pterula and Deflexula species were collected from Costa Rica,
Trinidad, Puerto Rico, New Zealand, Taiwan and Louisiana
(USA). All but two Pterula and Deflexula species were found
growing on either decomposing leaves or wood. Pterula cf.
tenuissima was isolated from within photosynthetic leaves of
Magnolia grandiflora using a standard protocol for the isolation of
endophytic fungi (Schulz et al. 1993). The mushroom collection
identified as UGM011206-01 was found growing on vegetative
mycelia grown by Apterostigma dentigerum ants.
Vouchers for Pterula and Deflexula collections (except D. sub-
simplex) are in the University of Minnesota Herbarium, James Ford
Bell Museum of Natural History, and cultures are in the Mycolo-
gical Culture Collection, Department of Plant Biology, University
of Minnesota. The substrates and geographical origins of the iso-
lates of the ant-grown fungal cultivars and other taxa have been
described elsewhere (Moncalvo et al. 2002; Villesen et al. 2004).
(b) DNA sequencing
Genomic DNA was extracted from lyophilized mushrooms or
vegetative mycelia using CTAB (hexadecyltrimethyl-ammonium
bromide) in a standardized DNA extraction protocol (Zolan &
Pukkila 1986). Genomic DNA was used as the template for PCR
amplification of the first 900 base pairs of the large subunit of the
nuclear ribosomal DNA gene. The PCR product was generated
using the LR0R and LR5 primers, and forward and reverse
sequences were obtained with the LR0R, LR3R, LR16 and LR5
primers (Moncalvo et al. 2002). Sequence data for UGM011206-
01 and the Pterula and Deflexula isolates (except D. subsimplex,
which was collected by other researchers and deposited in Gen-
Bank) were generated using dye-labelled dideoxy terminator cycle
sequencing (Applied BioSystems, Inc.) and an ABI 377 auto-
mated DNA sequencer. Contiguous sequences were edited with
S
EQUENCHER 3.0 (GeneCorps, Inc.) and are available at GenBank
(http://www.ncbi.nlm.nih.gov/GenBank/index.html; accession
numbers AY458121–AY458133).
In addition to the sequence data collected for this study,
sequences for the following taxa were obtained from GenBank
(accession numbers): D. subsimplex (AJ406572); fungal cultivars
grown by ants in the A. pilosum group (AY367613–AY367633);
Gerronema strombodes (AF261365); G. subclavatum (U66434);
Megacollybia platyphylla (AF261366); Clitocybula oculus
(AF261367); Hydropus fuliginarius (AF261368); Porotheleum fim-
briatum (AF261370); Marasmius fulvoferrugineus (AF261584);
Chaetocalathus liliputianus (AF261346); Crinipellis maxima
(AF042630); Tetrapyrgos nigripes (AF261337); and Campanella
sp. (AF261339).
(c) Phylogenetic analyses
Sequences for Pterula and Deflexula species were aligned by eye
within the euagarics dataset (Moncalvo et al. 2002) using PAUP
(Swofford 2002). A neighbour-joining (NJ) analysis of 902
sequences identified their close relatives. Sequences for Pterula
and Deflexula species and their closely related taxa were then
aligned to generate a trimmed dataset for maximum-parsimony
(MP) and Bayesian analyses. The tetrapyrgoid taxa were desig-
nated as the outgroup in analyses of the final dataset, which con-
sisted of 901 nucleotide sites. The data matrix of the final dataset
is available on request from A.B.M.
MP analysis was conducted with character-state changes weigh-
ted equally and gaps scored as ‘missing’. Branch-support values in
the MP phylogenies were obtained with 1000 replicates of non-
parametric bootstrap analyses in PAUP
. Bayesian analyses were
conducted using M
RBAYES 2.01 (Huelsenbeck & Ronquist
2001) with the general time-reversible model of nucleotide sub-
stitution; some sites were assumed to be invariable and variable
sites were assumed to follow a discrete gamma distribution
(GTR þ C þ I model); this was the best-fit model according to
M
ODELTEST v. 3.04 (Posada & Crandall 1998). Starting with a
random tree, four incrementally heated Markov chains in a
Markov chain Monte Carlo sampling method were used for
1 10
6
generations, sampling a tree every tenth generation to
ensure that successive samples were independent. Out of the
100 000 sampled trees, the trees that preceded convergence of the
Markov chain were discarded. From the remaining trees a 50%
majority-rule consensus tree was generated in PAUP
. Statistical
support for branches is represented by the percentage in which the
divergence is observed in the sampled trees (the posterior prob-
ability). Three independent Bayesian analyses were conducted to
identify congruent results of individual analyses.
3. RESULTS
Based on a NJ phylogenetic analysis, the cultivar grown by
the A. pilosum group was classified in the phylum Basidio-
mycota in the euagarics clade, along with the lepiotaceous
cultivars grown by all other fungus-growing ants (figure 1).
However, there was a great genetic distance between the
A. pilosum cultivar and the lepiotaceous cultivars (figure 1).
The euagarics clade comprises primarily gilled mushrooms
together with several non-gilled forms not traditionally
classified with gilled mushrooms (Moncalvo et al. 2002).
The NJ phylogeny of the euagarics dataset (n ¼ 912 taxa;
figure 1) and the MP and Bayesian analyses of the trimmed
dataset (n ¼ 46 taxa; figure 2) strongly indicated that 21
isolates of the A. pilosum cultivar were sister to a mono-
phyletic group of coral mushrooms in the genera Pterula
and Deflexula. Independent Bayesian analyses produced
the same majority-rule consensus tree, which was topologi-
cally identical to the two equally parsimonious trees
derived from the MP analysis (164 parsimony-informative
characters, length of 461, consistency index of 0.579,
retention index of 0.85).
In addition, examinations of over 300 gardens main-
tained by ants in the A. pilosum group led to the collection
of clusters of 1 0.25 mm pale-yellow coral mushrooms
(collection number UGM011206-01; figure 2a) growing
on a cultivar in an A. dentigerum nest in Panama. The
dimitic skeletal hyphae of these coral mushrooms were
characteristic of Pterula and Deflexula (Corner 1950) and
confirmed the taxonomic association as either Pterula or
Deflexula. However, the absence of spores prevented
1778 A. B. Munkacsi and others Convergent coevolution in fungus-growing ant symbiosis
Proc. R. Soc. Lond. B (2004)
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Apterostigma pilosum
cultivar
lepiotaceous cultivars
}
}
euagarics clade
0.005 substitutions/site
Figure 1. A NJ phylogeny illustrating the evolutionary relationships of ant-cultivated fungi within the euagarics clade. All fungus-
growing ants, except those in the Apterostigma pilosum group, grow one of three lepiotaceous cultivars. The A. pilosum cultivar is
clearly paraphyletic to the lepiotaceous cultivars and thus the only ancient phylogenetic divergence in the coevolutionary
interactions between the fungus-growing ants, their fungal cultivars and cultivar-infecting parasites (Currie et al. 2003).
Convergent coevolution in fungus-growing ant symbiosis A. B. Munkacsi and others 1779
Proc. R. Soc. Lond. B (2004)
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identification to genus and species level. Phylogenetic
analyses placed these coral mushrooms within the pterula-
ceous cultivar clade (figure 2).
4. DISCUSSION
Using broad taxon sampling, including the first mushroom
collected in a nest maintained by a species in the A. pilosum
group, we present molecular and morphological evidence
that showed the cultivar grown by the A. pilosum group was
domesticated from fungi in the coral-mushroom family
Pterulaceae. Pterula and Deflexula are the most speciose
genera in the enigmatic primarily tropical Pterulaceae
(Corner 1950, 1970; Kirk et al. 2001).
Prior to this study, only four genera of coral mushrooms
were classified in the euagarics clade, and none of these was
related to the cultivar grown by the A. pilosum group
(Hibbett & Binder 2002; Moncalvo et al. 2002). The sister
group of the pterulaceous cultivar þ Pterula þ Deflexula
clade includes the gilled mushrooms that were previously
identified as the closest relatives of the cultivar (figure 2;
Chapela et al. 1994; Moncalvo et al. 2002; Villesen et al.
2004). Chapela et al. (1994) predicted that the cultivar was
a member of the gilled-mushroom family Tricholomata-
ceae. However, they included only gilled mushrooms in
their study, since they were unaware that some non-gilled
morphologies were derived from the gilled morphology
(Hibbett et al. 1997). Moncalvo et al. (2002) sampled every
group previously reported to be in the euagarics as well as
taxa not predicted to be in the euagarics. Villesen et al.
(2004) sampled taxa previously reported to be related to
the A. pilosum cultivar. In all cases, gilled mushrooms in
Tricholomataceae were predicted to be the free-living rela-
tives of the cultivar.
In addition to finding the sister relationship between the
pterulaceous clade and the A. pilosum cultivar, we classified
a Pterula or Deflexula mushroom in the cultivar clade (fig-
ure 2). This mushroom was found growing on a cultivar
farmed by A. dentigerum ants. Although it cannot be ident-
ified unambiguously as the mushroom of the cultivar
domesticated by the A. dentigerum ants, several observa-
tions of that A. dentigerum nest suggest that it was the
mushroom of the pterulaceous cultivar. Several mush-
rooms were chewed on by the A. dentigerum ants, parallel-
ing the suppression of cultivar fruiting seen in nests of the
lepiotaceous cultivars (Mueller 2002). In addition, the nest
was queenless and had fewer than the average number of
workers (11 workers and five alates). Queenlessness
has been suggested to be a precondition for fruiting in the
lepiotaceous cultivar, indicating that the cultivar in the
A. dentigerum colony may have switched from an asexual
existence in a formerly queenright colony to sexuality upon
queen loss (Mueller 2002). Such a switch to sexuality is
predicted because only queenright nests produce new
foundress queens that can disperse the fungus to new nest
locations, and queen loss thus terminates this avenue of
reproduction for the cultivar.
(a) Convergent coevolution
The phylogenetic divergences that resulted in the three
major lineages of fungus-growing ants are reflected in the
phylogenies of the three lepiotaceous cultivars and the
parasites associated with the lepiotaceous cultivars, illus-
trating a strong pattern of parallel coevolution (Currie et al.
2003). However, parallel coevolution is not the only mode
of coevolution in the fungus-growing ant system.
From our study, it is clear that the pterulaceous cultivar
has an independent origin and is distantly related to the
three lepiotaceous cultivars. However, the overall assembly
of the four symbionts and their functional interactions are
the same for the pterulaceous and lepiotaceous cultivars,
suggesting a pattern of convergent coevolution in the
fungus-growing ant system. Each cultivar is grown by
particular ant species that use particular bacteria (Pseudo-
nocardia spp.) to minimize the growth of particular garden
parasites (Escovopsis spp.) on the cultivars (Currie et al.
2003; M. J. Cafaro and C. R. Currie, personal communi-
cation). To determine the processes leading to this conver-
gence, we must first understand the origin of the
interaction between the pterulaceous cultivar and the
Apterostigma ants. Several hypotheses for the origin of the
lepiotaceous cultivars have been proposed and tested
(Mueller et al. 1998; reviewed by Mueller et al. 2001).
There is no support for any of these hypotheses regarding
the origin of the pterulaceous cultivar.
We propose that the A. pilosum group inadvertently
domesticated the pterulaceous cultivar, which then dis-
placed the cultivar originally grown by these ants. The new
cultivar originated from either: (i) mycelia within material
used to fertilize the previous cultivar; (ii) mycelia within or
adjacent to the substrate of the ants’ nests; or (iii) spores.
The A. pilosum group constructs their gardens under or
inside decomposing logs and fertilizes their gardens with
wood fragments, dead plant debris and insect faeces
(Mueller et al. 2001; Villesen et al. 2004). The ants in the
A. pilosum group use wood to grow their fungal cultivar
much more frequently than do any of the other fungus-
growing ants (Villesen et al. 2004). Many Pterula and all
Deflexula species are wood inhabiting (Corner 1950, 1970).
Therefore, encounters between the ancestral pterulaceous-
cultivating ant species and Pterulaceae species would be
probable. The rare use of wood to grow lepiotaceous culti-
vars is consistent with the non-wood substrates of the free-
living relatives of the lepiotaceous cultivars and the poor
ability of the lepiotaceous cultivars to degrade cellulose
(Gomes de Siqueira et al. 1998; Abril & Bucher 2002).
Although the enzymatic potential for wood decay by the
pterulaceous cultivar has yet to be investigated, a closely
related species, Pterula echo, has been grown in axenic
Figure 2. (Opposite.) The evolutionary relationships of the
Apterostigma pilosum cultivar and coral mushrooms in Pterula
and Deflexula. This phylogeny is one of two equally
parsimonious trees derived from a MP analysis and is
topologically identical to the majority-rule consensus tree
derived from Bayesian analyses. (a–e) Photographs of the
mushrooms connected to the corresponding taxa by dashed
lines. (a) UGM011206-01 is a Pterulaceae species mushroom
collected in a garden maintained by ants in the A. pilosum
group. (e) Megacollybia platyphylla is a representative of the
gilled mushrooms that were previously predicted to be the
free-living relatives of the A. pilosum cultivar. Bootstrap values
(> 70) and posterior probability values (> 95) are indicated
above and below nodes, respectively. Coloured boxes indicate
the country of origin for isolates of selected taxa (GU, Guyana;
PA, Panama; NZ, New Zealand; TR, Trinidad; CR, Costa
Rica; PR, Puerto Rico; USA, United States of America; TA,
Taiwan). Scale bars, 1 mm.
1780 A. B. Munkacsi and others Convergent coevolution in fungus-growing ant symbiosis
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(a)
GU
GU
GU
GU
PA
PA
PA
PA
PA
PA
PA
PA
PA
PA
PA
PA
PA
PA
PA
PA
PA
PAPA
NZ
NZ
NZ
TR
CR
CR
PR
CR
CR
CR
CR
USA
TA
g39
s326
pv408
pv430
pv431
pterulaceous cultivar
Pterula + Deflexula
s204
g56
g58
pv407
pv409
pv410
pv411
pv412
g51
UGM011206-01
s21
s44
pv403
pv406
s91
s86
pv426
Deflexula fascicularis
Pterula cf. debilis
Pterula cf. debilis
Pterula echo
Pterula aff. epiphylloides
Pterula aff. epiphylloides
Pterula cf. navicula
Pterula cf. caricis-pendulae
Pterula sp. nov.
Pterula sp. nov.
Deflexula nana
Pterula cf. tenuissima
Deflexula subsimplex
Gerronema strombodes
Gerronema subdavatum
Megacollybia platyphylla
Clitocybula oculus
Hydropus fuliginarius
Porotheleum fimbriatum
Marasmius fulvoferrugineus
Chaetocalathus liliputianus
82
99
100
100
100
81
100
100
97
Crinipellis maxima
Tetrapyrgos nigripes
100
85
100
100
100
100
100
84
97
94
97
99
100
100
100
100
100
95
98
96
98
75
100
100
100
100
81
84
71
Campanella sp.
5 changes
(d)
(e)
(c))
(b)
Figure 2. (Caption opposite.)
Convergent coevolution in fungus-growing ant symbiosis A. B. Munkacsi and others 1781
Proc. R. Soc. Lond. B (2004)
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culture on wood (McLaughlin & McLaughlin 1980). The
maintenance of this trait would enhance the growth rate of
the pterulaceous cultivar in gardens fertilized with wood
fragments. The pterulaceous cultivar may also have origi-
nated as a saprobe or an endophyte, as suggested by our
isolation of the first endophytic coral mushroom, Pterula cf.
tenuissima. It is also possible that spores borne on Pterula or
Deflexula mushrooms were introduced to the garden via
wind or on material used to fertilize the garden. Whether
the pterulaceous cultivar originated within or adjacent to
the original garden, the ancestral pterulaceous fungus sur-
vived the extensive physical and chemical processing of
garden fodder by the ants (Currie & Stuart 2001) and poss-
ibly displaced the original cultivar.
The quadripartite symbiosis between A. pilosum ants,
their pterulaceous cultivar, the antibiotic-producing
Pseudonocardia species and the Escovopsis species that para-
sitize the pterulaceous cultivar is as highly coevolved as the
interactions of the other ant–cultivar–parasite–bacterium
symbioses, despite having a different evolutionary history.
The evolutionary histories of the A. pilosum ants and the
Escovopsis species are more similar than the evolutionary
histories of the A. pilosum ants and the pterulaceous cultivar
(Currie et al. 2003). This suggests that the ants may have
introduced the parasite and bacteria to the novel cultivar.
However, this phylogenetic pattern does not rule out the
possibility that the pterulaceous cultivar originated at the
same time as fungiculture in the A. pilosum group,
suggesting that all the interactions in the quadripartite
symbiosis could have arisen independently. Additional col-
lections of Pterulaceae species and the pterulaceous culti-
var from their common habitats, ranging from Argentina to
Mexico, will help determine the phylogenetic, geographical
and ecological origins of the pterulaceous cultivar. These
data will allow a reconstruction of the symbiosis and serve
as a foundation for understanding the convergence of
coevolutionary interactions.
The authors thank E. McLaughlin for collecting and culturing
Pterula and Deflexula, G. Weiblen for photographing
UGM011206-01, J.-M. Moncalvo for providing the euagarics
dataset prior to publication, and R. Kasili for isolating the
endophytic Pterula cf. tenuissima. Suggestions from two anony-
mous reviewers improved this manuscript. Funding was pro-
vided by the National Science Foundation (DEB-0090301 to
A.B.M., M.B. and D.J.M., DEB-9983879 and DEB-0110073
to U.G.M., DEB-0072741 to M.B., and DEB-9306578 to
D.J.M.), the University of Aarhus (Biological Institute and the
Faculty of Natural Sciences grants to P.V.) and the University
of Minnesota (Minnesota Agricultural Experiment Station
and a Bush Sabbatical Fellowship to D.J.M.). J.J.P. was sup-
ported by a NSF Postdoctoral Fellowship in Microbial
Biology during the preparation of this manuscript.
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