Behav Ecol Sociobiol (2003) 53:65–71
DOI 10.1007/s00265-002-0559-y
REVIEW
Judith Korb · Duur K. Aanen
The evolution of uniparental transmission of fungal symbionts
in fungus-growing termites (Macrotermitinae)
Received: 27 September 2002 / Revised: 23 October 2002 / Accepted: 26 October 2002 / Published online: 4 December 2002
© Springer-Verlag 2002
Abstract Mutualistic associations between different organisms are theoretically expected when the interests of
independently reproducing units are aligned to form a
single reproductive unit. This alignment does not come
about easily, because models show that hosts and symbionts can be in conflict over the transmission of symbionts. Selection will favour hosts that are able to limit genetic variation of symbionts, for example by enforcing
uniparental vertical transmission, while symbionts will
be selected to disperse independently of the host. A crucial factor determining the evolution and elaboration of
symbiotic relationships is therefore who controls the
transmission of symbionts. In the fungus-growing termites (Macrotermintinae) horizontal transmission seems
to be the rule as the termites normally acquire their cultivated fungus (Termitomyces) from the environment. In
spite of this general pattern, uniparental, vertical transmission has evolved in two unrelated Macrotermitinae
genera, where only one sex of the two primary reproductives carries asexual spores from the fungal comb of its
parent colony to inoculate the new fungus comb. Remarkably, symbiont transmission is exclusively paternal
in Macrotermes bellicosus, whereas symbionts are maternally inherited in all Microtermes species studied so
far. Thus, in Macrotermitinae horizontal transmission is
the ancestral state with two independent origins to uniparental, vertical transmission. This is in contrast to fungus-growing ants where uniparental, vertical transmission is the rule. Causes and consequences of this difference are further discussed. Despite this fundamental difference both groups evolved a similar symbiosis that is
Communicated by A. Cockburn
J. Korb (✉)
Biologie I, Universität Regensburg, 93040 Regensburg, Germany
e-mail: judith.korb@biologie.uni-regensburg.de
Tel.: +49-941-9432461, Fax: +49-941-9433304
D.K. Aanen
Department of Population Ecology, Zoological Institute,
University of Copenhagen, Universitetsparken 15,
2100 Copenhagen, Denmark
probably the key for their ecological success: the fungusgrowing ants in the neotropics and the fungus-growing
termites in the paleotropics.
Keywords Evolutionary conflict · Host symbiont
conflict · Mutualism · Symbiosis · Termitomyces
Introduction
Mutualisms are best viewed as reciprocal exploitations
that nonetheless provide net benefits to each partner
(Herre et al. 1999). This view implies that there is no
qualitative distinction between “truly parasitic” and “truly mutualistic” interactions, but that the degree of mutualism in symbiotic relationships can be considered as a
continuous variable. Among the factors that have been
thought to promote more mutualistic interactions is genetic homogeneity of symbionts (e.g. Herre et al. 1999).
Symbiont fitness has two components: one arises from
the overall success of the group of symbionts within a
host, and the other originates from the competitive success and transmission relative to other symbionts within
the same host. As relatedness declines within hosts, a
genotype’s success depends more on its ability to outcompete its neighbours and less on the overall success of
the group (Hamilton 1972). Thus, declining relatedness
of symbionts should favour them to compete more intensely. This intense competition is likely to decrease the
overall success of the group of symbionts and to have
virulent side-effects on the host. Therefore, it is in the interest of hosts to keep symbionts genetically homogeneous. One way to achieve this is to reduce mixing of symbionts by clonal and vertical uniparental transmission
(Frank 1996). The synthetic model by Frank (1996)
arose from a precursor that addressed the evolution of
uniparental inheritance of cytoplasmic elements like mitochondria and chloroplasts (Cosmides and Tooby 1981;
for a recent review see Hurst et al. 1996). Recently, the
theory has also been applied more generally to mutualistic relationships (Frank 1996; Herre et al. 1999). Before
66
continuing, it is useful to define some terms used
throughout this paper. Speaking about transmission
modes we have to distinguish between vertical-horizontal versus clonal-sexual transmission. Vertical symbiont
transmission is transmission of symbionts from host
parent to host offspring. That is, reproduction of symbionts is aligned with reproduction of the host. Vertical
transmission can be uniparental (via one of the two sexes) or biparental (via both sexes). Horizontal symbiont
transmission, on the other hand, is transmission of symbionts independently of host reproduction. Such horizontal transmission will often result in associations between
symbionts and hosts outside the parental host lineage.
Both horizontal and vertical transmission can be either
clonal (i.e. no genetic recombination occurs between
symbionts) or sexual (i.e. recombination occurs), but in
many cases vertical transmission is clonal, whereas horizontal transmission is sexual.
Hoekstra (1987) has pointed out a conceptual problem
with the evolution of host control over cytoplasmic mixing, and this complication persists in the more general
model of host control of symbiont transmission (Frank
1996). The benefit of restricted mixing is a delayed benefit to the mean fitness of the host population rather than
to the individual host, whereas the evolution of host control over symbiont transmission requires that individual
hosts gain immediate advantages. For cytoplasmic elements several such immediate advantages have been proposed (e.g. Hoekstra 1990; Hurst 1990) and similar advantages probably apply to many other host-symbiont interactions. Frank (1996) has proposed several possibilities for a direct association between reduced mixing of
symbionts and reduced virulence of symbionts to the
host. One such possibility is that the level of competitiveness between symbionts (correlated with the level of
virulence) is not a genetically fixed trait but a plastic
trait that is expressed in response to increased levels of
genetic variation between symbionts.
However, to some extent the symbionts have different interests to the hosts (Frank 1996). Selection favours symbionts to disperse out of the host-imposed
vertical host lineage, even if such horizontally dispersing symbionts have a very low chance of successful establishment (Hamilton and May 1977). Hamilton and
May’s (1977) model shows that horizontal transmission
is favoured to avoid competition with relatives. Horizontal transmission will result in symbiont mixing and
reduced relatedness among symbionts in the same host,
favouring the evolution of virulent characteristics, as
outlined earlier.
These considerations show that hosts and symbionts
can easily be in conflict over the patterns of transmission. Hosts will be selected to reduce mixing by imposing vertical transmission of symbionts, whereas symbionts will be selected to realise at least some horizontal
transmission. The degree to which a host can control the
inheritance of its symbionts is therefore one of the determinants of the degree of mutualism to which a symbiosis
can evolve (Frank 1996; Herre et al. 1999).
In this paper we review the currently available data
on the largely horizontal transmission of fungal symbionts in the termite subfamily Macrotermitinae. We develop a hypothetical framework to explain the evolution
of the observed transmission patterns based on the above
considerations and we compare fungus transmission in
termites with fungus transmission in fungus-growing
ants, where vertical transmission is the rule. We suggest
explanations for the differences between these two major
groups of social insects that independently evolved fungus-rearing and illustrate the value of both systems as
model systems for host-symbiont evolution.
The fungus-growing termites
A single subfamily of higher termites, the Macrotermitinae, has established an ectosymbiotic relationship with
basidiomycete fungi of the genus Termitomyces (for a recent review see Rouland-Lefèvre 2000; Aanen et al.
2002). These fungi are cultivated within the nest in convoluted, greyish-brown combs that consist of plant material (for details see Traniello and Leuthold 2000). Macrotermitinae digest diverse types of cellulose-rich food
such as wood and leaf litter, partially with their own
cellulose digesting enzymes (Abo-Khatwa 1978; Martin
and Martin 1978, 1979; Rouland et al. 1988; Veivers
et al. 1991; Rouland-Lefèvre 2000). The fungus-growing
termites and the fungi appear to be obligately dependent
on each other (Batra and Batra 1966; Johnson 1981).
Wood and Thomas (1989), Veivers et al. (1991) and
Darlington (1994) list several benefits of fungus cultivation to both the termites and the fungus. For the termites
some of the benefits are that (1) the fungi degrade chemically complex substances (e.g. lignin) into substances
that can be used by the termites and (2) the fungi increase the N:C ratio of the termites’ diet, and allow them
to exploit more diverse cellulose sources than most other
termites are able to use. The fungi gain advantages in (1)
access to plant material that can easily be penetrated and
has an increased surface area, (2) the provision of an optimal microclimate, and (3) the selective inhibition of
other fungi that are competitively superior and the prevention of microbial infections by termite secretions.
The close association between Macrotermitinae and
Termitomyces seems to be the result of a long coevolutionary process which has a single African origin with a
lack of secondary domestications of other fungi or reversal of mutualistic fungi to a free-living state (Aanen et al.
2002). Some distinct traits of the termites and their
fungi are likely to be a direct consequence of this long
coevolution. For example, elaborate thermoregulation in
nests of the Macrotermitinae (Lüscher 1961; Korb and
Linsenmair 1999, 2000a, 2000b) leads to constantly high
temperatures and to high relative humidity, providing the
optimal microclimate for cultivation of the fungi (Wood
and Thomas 1989). Furthermore, complementary enzyme
systems exist in some associations where cellulosedigesting enzymes derived from both the termites and
67
the fungus interact synergistically (Rohrmann 1978;
Martin and Martin 1978, 1979; Rouland et al. 1988; see
also Veivers et al. 1991).
Fungus transmission in termites
Observed transmission modes
In most Macrotermitinae-Termitomyces associations that
have been studied horizontal transmission of fungus occurs (Table 1, Fig. 1a). There is thus no alignment of interest of the two independently reproducing entities, the
termites and the fungus, as is illustrated in Fig. 1a by the
two separate life-cycles. The fungus produces fruiting
bodies (basidiocarps) with sexual spores; these spores
are carried into newly founded nests by the first workers
of the new colony on their first foraging trips (Johnson
1981; Johnson et al. 1981; Darlington 1994). Laboratory
experiments have shown that alates (winged sexuals) fail
to establish a colony unless they are supplied with an external source of fungal spores (Johnson 1981; Johnson et
al. 1981; Sieber 1983). Interestingly, the fruiting of the
fungus seems to be synchronised with the emergence of
the first fully developed foraging workers in newly
founded colonies (Johnson et al. 1981).
However, a few species of Macrotermitinae have
developed vertical, uniparental symbiont transmission
(Table 1) with an alignment of the reproductive units of
the termite and the fungus (illustrated by a single lifecycle in Fig. 1b). In the five species of Microtermes
studied and in Macrotermes bellicosus alates of one sex
carry a bolus of conidia (asexual spores) in their foregut
from the fungus combs of the parent colony to inoculate
the first fungus combs in their newly founded colonies
(Fig. 1b; Johnson 1981; Johnson et al. 1981; Sieber
1983; Wood and Thomas 1989). In line with this observation, laboratory experiments have shown that these
species can establish a colony (with a fungal comb)
without the addition of fungal spores (Johnson 1981;
Johnson et al. 1981; Sieber 1983). In Macrotermes
bellicosus the males transmit the fungus whereas the females transmit the fungus in Microtermes spp. Fruiting
bodies have never been observed for the fungi associated
Table 1 Modes of fungus
transmission in several Macrotermitinae species
Fig. 1a, b Transmission of fungus in Macrotermitinae during colony foundation. Text in italics: fungus life-cycle; regular text: termite life-cycle. a Horizontal transmission. Alates found new colonies. The first workers collect sexual spores of fruiting fungus during their foraging trips and inoculate new fungus combs. Thus, the
fungus combs most probably consist of a mixture of different mating types, so that sexual reproduction of fungi is possible. b Vertical, uniparental transmission. One sex of the alates of the termites
carries asexual fungus spores to inoculate new fungus combs during colony foundation. This results in a lack of different mating
types in the fungus so that sexual reproduction of the fungus is not
possible
with these termite species (Johnson et al. 1981; Darlington
1994; Korb, unpublished observations), as expected if
transmission is exclusively vertical (see later). The difference in sex-specificity in fungus transmission indicates an independent origin of uniparental, vertical transmission in both groups. This is supported by molecular,
phylogenetic investigations; termites with vertical transmission do not form a monophyletic group, but belong to
two unrelated clades (Aanen et al. 2002). This strongly
Species
Transmission mode
References
Ancistrotermes guineensis
A. crucifer
A. cavithorax
Pseudacanthotermes spiniger
Macrotermes subhyalinus
M. michaelseni
Odontotermes pauperans
O. smeathmani
O. montanus
Macrotermes bellicosus
5 species of Microtermes
Horizontal transmission
Horizontal transmission
Horizontal transmission
Horizontal transmission
Horizontal transmission
Horizontal transmission
Horizontal transmission
Horizontal transmission
Horizontal transmission
Vertical transmission, male
Vertical transmission, female
Sands 1960
Johnson et al. 1981
Johnson et al. 1981
Johnson et al. 1981
Johnson et al. 1981
Sieber 1983
Johnson et al. 1981
Johnson et al. 1981
Sieber 1983
Johnson et al. 1981
Johnson 1981
Johnson et al. 1981
68
Fig. 2 The life cycle of Termitomyces with different transmission
modes. Outside the main circle, is the life cycle of a fungus that is
horizontally transmitted as indicated. For these horizontally transmitted fungi, monokaryotic spores (basidiospores, 1n) can be carried into a new termite nest by foraging workers. These spores
germinate and give rise to a monokaryotic mycelium with haploid
nuclei (monokaryon). Two monokaryons belonging to the same biological species, and having opposite mating types, can fuse and
form a stable dikaryotic mycelium (dikaryon), all cells of which
have two haploid nuclei (n+n). Dikaryons can form fruiting bodies, or mushrooms. In these mushrooms, basidia are formed,
where nuclear fusion takes place (giving rise to a short diploid
stage, 2n), followed by meiosis and spore formation. Inside the
main circle, the potential cycles of a vertically transmitted fungus
are drawn. For these fungi, the horizontal route is blocked (parallel lines) at either 1 (no fusion of monokaryons) or 2 (termites prevent fruiting of dikaryon by eating primordia). In 1, there is clonal
propagation by alates of the monokaryotic stage (small cycle 1),
whereas in 2 there is clonal propagation of the dikaryotic stage
(small cycle 2). See text for more details
suggests that horizontal transmission is the ancestral
transmission mode and that uniparental transmission is a
derived trait with two independent origins.
Fungal life cycles and transmission
To our knowledge life cycles of Termitomyces have not
been studied in any detail. It is usually assumed that
Termitomyces fungi have a heterothallic (i.e. outcrossing) life cycle (Heim 1977), like most basidiomycetes
studied so far (Raper 1966). In this life cycle (Fig. 2)
spores germinate and form a monokaryon, all cells of
which have a single nucleus. Two monokaryons of the
same species with different mating types can fuse and
form stable dikaryon, all cells of which have two nuclei,
one of each monokaryon. A dikaryon can form fruiting
bodies, where meiosis and spore formation takes place.
The fruiting symbionts of Macrotermitinae with a horizontal transmission are likely to fit into this general
scheme. The four-spored basidia of fruiting bodies from
Termitomyces support this (Heim 1977). Alternatively,
however, some of the fruiting Termitomyces fungi might
have a (secondarily) homothallic (i.e. non-outcrossing)
mating system. In that case, a single fungal spore is sufficient to complete a fungal life cycle.
What type of life cycle do the non-fruiting Termitomyces species have? One possibility is that the mycelium
of these species is monokaryotic and that this monokaryotic mycelium is clonally propagated by vertical transmission (possibility 1 in Fig. 2). Very few monokaryotic
basidiomycetes that can produce fruiting bodies are
known (e.g. Ullrich and Raper 1975). Therefore, keeping
mycelia monokaryotic could be a proximate explanation for the lack of fruiting of some fungal symbionts.
Another possibility is that the non-fruiting fungi have a
dikaryotic mycelium that is clonally transmitted by vertical transmission. In this case, the termites might actively
prevent their fungal symbionts from fruiting, for example by eating the primordia (possibility 2 in Fig. 2). Obviously, life cycles of Termitomyces need to be studied to
test these different possibilities.
Possible advantages of vertical, uniparental transmission
As explained in the Introduction, vertical uniparental
symbiont transmission is expected in the long-term to
lead to relatively mutualistic traits of the symbiont fungi,
which is obviously in the interest of the host. We hypothesise that there are also several direct advantages
for the termites to this mode of transmission so that
Hoekstra’s (1987) delayed benefit argument does not apply. Some of these advantages are intrinsic to the vertical
transmission itself while other advantages are directly a
consequence of the uniparental aspect of the transmission. An obvious advantage of vertical transmission over
horizontal transmission is that there is a greatly reduced
risk that a new colony fails to establish a fungus comb if
there is no fruiting fungus near the new colony. However, this advantage of vertical transmission for the host
does not explain why the conidia are transmitted by only
one sex. Avoidance of mixed fungal inoculations might
have several immediate advantages for fungus-growing
termites. In the Basidiomycetes genetically different dikaryons show strong incompatibility reactions (Rayner et
al. 1984; for an overview, see Worrall 1997) and monokaryons of the same mating type also show different
types of incompatibility reactions (Rayner et al. 1984).
These incompatibility reactions result in strongly reduced mycelial growth in zones where the fungi meet.
Therefore, termites that avoid mixed fungal inoculations
will have a selective advantage over termites that do not.
Another potential advantage of avoidance of mixed infections is a reduction in the horizontal spread of genetic
elements, such as plasmids, transposable elements and
viruses. Such elements can reduce fitness of fungi significantly (Van Diepeningen et al. 1997). Apart from these
advantages related to vertical and uniparental transmission, we also expect that the host benefits from preventing its fungus from fruiting, i.e. from investing resources
in costly fruiting bodies.
69
Table 2 The two main models that have been proposed for the
successive evolution of fungus agriculture in social insects (after
Mueller et al. 2001). There is some evidence that the “transmis-
sion first” model applies to the attine ants. However for the fungus-growing termites a “consumption first” model is more likely.
See text for more details
Traditional “consumption first” model
Consumption →
Fungi are part of diet
Cultivation →
Insects cultivate fungus by adding substrate
Transmission
Vertical fungus transmission
Alternative “transmission first” model
Transmission →
Specialised fungi dispersed by insect
Consumption →
Fungi become part of insect diet
Cultivation
Insects cultivate fungus by adding substrate
Comparison with attine-fungus mutualism
Horizontal transmission of fungal symbionts is the most
widespread mode of fungal transmission in fungus-growing termites. It has been shown for the genera Ancistrotermes, Pseudacanthotermes, Macrotermes and Odontotermes, and the common occurrence of fungal fruiting in
other genera (except Microtermes) suggests that it also
exists in those genera. Horizontal transmission has been
shown to be the ancestral state with two independent
transitions to uniparental, vertical transmission (Aanen et
al. 2002). In the genus Microtermes this transition led to
fungal transmission by the female reproductive, and in
Macrotermes bellicosus the male reproductive became
the transmitter.
It is possible that the two transitions in the Macrotermitinae from horizontal symbiont transmission to uniparental vertical transmission have gone via an intermediate stage of biparental vertical transmission, but so far
no examples of this intermediate stage of transmission
have been found in the relatively few species that have
been studied. However, this stage might be short-lived
because of the fitness disadvantages associated with
mixed fungal inoculations for the termite hosts as discussed before. The question remains though, how species with horizontal acquisition of fungi cope with problems associated with mixed infections. In Table 2 the hypothesised evolution of transmission modes is summarised, together with some characteristics of each stage.
Fungus-growing ants or Attini (Formicidae, Myrmicinae) are comparable to the Macrotermitinae in having a
strong, obligate association with fungi (Basidiomycetes,
Agaricales, mainly Lepiotaceae), which they cultivate
and on which they depend for the nourishment of their
larvae (for more information see Weber 1972; Chapela et
al. 1994; Schultz and Meier 1995; Mueller et al. 1998).
In contrast to the Macrotermitinae, vertical uniparental
transmission probably occurs throughout the whole
group and may represent the ancestral state. However,
recent investigations have also shown that horizontal
transmission, for example via pleometrotical founding,
may occur in attine ants (Rissing et al. 1989; Mintzer
1990; Bekkevold et al. 1999; Adams et al. 2001; Green
et al. 2002) which explains why specificity across species is relatively low (Mueller et al. 1998). The traditional hypothesis for the origin of the attine ant-fungus mutualism is that consumption of certain fungi by the ants
was the first step. This step was followed by selective
cultivation and finally by selective transmission of these
fungi. More recently it has been hypothesised that the
ant-fungus mutualism started with transmission of specialised fungi by ants and that this initial step was followed by consumption and cultivation of these fungi by
the ants (Mueller et al. 2001). It is important to realise in
this context that ant colonies are normally founded by a
single individual, the queen. This makes vertical transmission of fungi automatically uniparental. In line with
the theory described in this paper, we expect an easier
evolution towards mutualism in such a situation of uniparental transmission by default.
In contrast, in termites vertical transmission would
initially have been biparental since a termite colony is always founded by two individuals of opposite sex. Thus
in termites we would not expect the evolution towards a
mutualistic association to start from vertical transmission. Rather, it is hypothesised that incidental consumption of fungi with decaying wood is the origin of fungusgrowing in termites since termites as primarily wood
feeders always lived in close contact with fungi (Wood
and Thomas 1989). Thus, for the Macrotermitinae it is
much more likely that consumption of fungi was the first
step, followed by cultivation. Ultimately, a few species
developed specialised vertical transmission modes, either
by males or by females. The phylogenetic analysis confirms this scenario (Table 2).
Despite these differences in the main transmission
mode and the likely evolution of the symbiotic association in fungus-growing ants and termites, both mutualisms have converged. Neither in the ant nor in the termite association are there strong associations between
the evolutionary history of the hosts and the symbionts.
Clades must repeatedly have exchanged their fungal
symbionts. Single host species have a variety of symbionts and the symbionts of different genera do not form
monophyletic groups. Specificity of fungal symbionts
occurs mainly at higher taxonomic levels (Chapela et al.
1994; Mueller et al. 1998; Aanen et al. 2002).
Recent molecular analyses have shown that in studies
of mutualisms a distinction can be made between ecological (from generation to generation) versus evolutionary
time scales (from lineage to lineage; Herre et al. 1999),
although the borderline between these time scales is not
always sharp. For example, even when vertical transmission is found over ecological time scales, rare horizontal
70
transfers can leave their traces. This has generally been
found for symbioses between Wolbachia bacteria and insects (e.g. Vavre et al. 1999) and has been inferred for
attine ants (Mueller et al. 1998; Bot et al. 2001). For the
Macrotermitinae that have evolved vertical fungus transmission, it has recently been shown that the fungi of the
two clades of species with vertical transmission do not
form two monophyletic groups, so that some horizontal
transmission must also have occurred here (Aanen et al.
2002).
These considerations show that fungus-growing social
insects are good model systems to test theories on the
evolution of mutualistic associations. Key questions to
address would be: Does mixing of symbionts have immediate costs to the host and what are these costs? Termite species with horizontal transmission seem to have
only one fungal strain in one nest (Aanen et al. 2002).
How do they obtain a single strain? Are associations
with horizontal transmission less mutualistic than associations with uniparental, vertical transmission? Clearly,
these systems can provide valuable insight into the evolution of mutualistic associations in general by testing
key assumptions.
Acknowledgements For discussions and comments on the manuscript we wish to thank Carl Anderson, Koos Boomsma, Mischa
Dijkstra, Jürgen Heinze, David Nash, Jes Søe Pedersen, and three
anonymous referees. J.K. was supported by an Emmy Noether
Fellowship of the DFG (Ko 1895/2–1). D.K.A. was financially
supported by an EU Marie Curie Fellowship (HPMF-CT-2000–
00642). Work supported in part by the European Community’s
Improving Human Potential Programme under contract HPRNCT-2000-00052, INSECTS.
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