Research Topics

Long live the queen: royal succession throughasexual reproduction in termites
The major advantage of sexual reproduction (over asexual
reproduction) is that it promotes genetic variability, despite the
obvious disadvantages of reduced genetic contribution to
offspring and the cost of finding mates. The benefits of sexual
reproduction can be reduced by inbreeding because inbreeding
lowers genetic diversity at both the individual and population
levels. Many termite species undergo royal succession, in which
the primary reproductives who found colonies (king and queen)
are replaced by secondary reproductives from within the nest.
Under normal sexual reproduction, such a breeding system is
expected to result in inbred colonies with limited genetic
diversity.

We found that the termite Reticulitermes speratusavoids
inbreeding by the conditional use of sexual reproduction and
parthenogenesis. We sampled mature field colonies and found
that in nearly all cases, primary kings were present but primary
queens had been replaced by an average of 55.4 secondary
queens. Genetic analysis showed that secondary queens were
almost exclusively produced parthenogenetically by the original
primary queen, whereas workers and alates (new primary
reproductives) were produced by sexual reproduction and
therefore retained levels of heterozygosity expected under
outbreeding. Moreover, by producing her replacements
parthenogenetically, the queen maintains her full genetic
contribution to the next generation of primary reproductives.
These findings reveal a novel breeding system in which asexually
produced replacement reproductives in colonies of a social
insect are used to boost sexual reproductive output of the
queen to the benefit of both the queen and the colony.


[Publication]

Matsuura, K., Vargo, E.L., Kawatsu, K., Labadie, P.E., Nakano, H.,
Yashiro, T.and Tsuji, K.: Queen succession through asexual
reproduction in termites.Science, 323: 1687 (2009).
A single primary king with many secondary queens in a mature colony of  Reticulitermes speratus.
Tetmite-egg mimicking fungus "Termite Ball"
Insects and fungi share a long history of association in various
habitats, including the wood-decomposition niche. Fungal
mimicry of termite eggs is one of the most striking evolutionary
consequences of insect?fungus association. Termites of the
genus Reticulitermes often harbor fungal sclerotia, called
“termite balls”, along with eggs, whereby the fungus gains a
competitor-free habitat in termite nests (Fig. 1). Sophisticated
morphological and chemical camouflage are needed for the
fungus to mimic termite eggs. In this talk, I would like to
demonstrate how the fungus mimics termite eggs so as to
control egg protection behavior of the termites. The fungus
mimics termite eggs chemically by producing the cellulose-
digesting enzyme beta-glucosidase (Fig. 2). We found that the
termite egg-recognition pheromone consists of beta-
glucosidase and lysozyme. Both enzymes are major salivary
compounds in termites and are also produced in termite eggs.
Termite balls were tended by termites only when the fungus
produced beta-glucosidase. Our results showed that the overlap
of the cellulose digestion niche between termites and the fungus
sharing the same chemicals provided the opportunity for the
origin of termite egg mimicry by the fungus. Our findings suggest
that pheromone compounds may have originally evolved within
other life history contexts, only later gaining function in
chemical communication. Egg mimicry, by which the fungus can
easily gain access to the centre of the nest, seems to be an
evolutionary loophole around anti-parasite defense in termites.

[Publication}
Reference
Matsuura, K., Yashiro, T., Shimizu, K., Tatsumi, S. and Tamura, T.:
Cuckoo fungus mimics termite eggs by producing the cellulose-
digesting enzyme beta-glucosidase. Current Biology, 19, 30-
36 (2009).
Matsuura, K., Tamura, T. Kobayashi, N., Yashiro, T. Tatsumi, S.:
The antibacterial protein lysozyme identified as the termite egg
recognition pheromone. PLoS ONE 2(8): e813. doi:10.1371/
journal.pone.0000813
Yashiro, T., Matsuura, K. : Distribution and phylogenetic analysis
of the termite-egg mimicking fungi “termite balls” in
Reticulitermes termites. Annals of the Entomological
Society of America 100(4), 532-538 (2007).
Matsuura, K: Termite-egg mimicry by a sclerotium-forming
fungus. Proceedings of the Royal Society B: Biological
Sciences 273, 1203-1209 (2006).
Matsuura, K., Tanaka, C. and Nishida, T.: Symbiosis of a termite
and a sclerotium-forming fungus: Sclerotia mimic termite eggs.
Ecological Research 15, 405-414 (2000)
Fig. 1 Termite balls in the egg pile of a termite Reticulitermes flavipes. Termite eggs are transparent and oval, while termite balls are brown and spherical.
Fig. 2 Detection of beta-glucosidase using a fluorescent probe Micrograph (upper panels) or fluorescent micrographs (lower panels) of a termite salivary gland, termite eggs dissected from the ovary of a queen, cross-section of the abdomen of a termite worker and termite balls harvested from a Potato Dextrose Agar (PDA) plate containing termite nest material. SG: salivary gland, SR: salivary reservoir, SD: salivary duct, HG: hind gut. Termite eggs and termite balls share beta-glucosidase, while no beta-glucosidase was present in the Argentine ant egg (in the square).

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