Abstract Mutualistic associations between different or-
ganisms 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 symbi-
onts can be in conflict over the transmission of symbi-
onts. Selection will favour hosts that are able to limit ge-
netic variation of symbionts, for example by enforcing
uniparental vertical transmission, while symbionts will
be selected to disperse independently of the host. A cru-
cial factor determining the evolution and elaboration of
symbiotic relationships is therefore who controls the
transmission of symbionts. In the fungus-growing ter-
mites (Macrotermintinae) horizontal transmission seems
to be the rule as the termites normally acquire their culti-
vated fungus (Termitomyces) from the environment. In
spite of this general pattern, uniparental, vertical trans-
mission has evolved in two unrelated Macrotermitinae
genera, where only one sex of the two primary reproduc-
tives carries asexual spores from the fungal comb of its
parent colony to inoculate the new fungus comb. Re-
markably, symbiont transmission is exclusively paternal
in Macrotermes bellicosus, whereas symbionts are ma-
ternally inherited in all Microtermes species studied so
far. Thus, in Macrotermitinae horizontal transmission is
the ancestral state with two independent origins to unipa-
rental, vertical transmission. This is in contrast to fun-
gus-growing ants where uniparental, vertical transmis-
sion is the rule. Causes and consequences of this differ-
ence are further discussed. Despite this fundamental dif-
ference both groups evolved a similar symbiosis that is
probably the key for their ecological success: the fungus-
growing 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 “tru-
ly mutualistic” interactions, but that the degree of mutu-
alism in symbiotic relationships can be considered as a
continuous variable. Among the factors that have been
thought to promote more mutualistic interactions is ge-
netic 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 suc-
cess 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 out-
compete its neighbours and less on the overall success of
the group (Hamilton 1972). Thus, declining relatedness
of symbionts should favour them to compete more in-
tensely. 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 in-
terest of hosts to keep symbionts genetically homogene-
ous. One way to achieve this is to reduce mixing of sym-
bionts 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 mi-
tochondria 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 mutualis-
tic relationships (Frank 1996; Herre et al. 1999). Before
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
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