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, 273 (1591), 1203-9

Termite-egg Mimicry by a Sclerotium-Forming Fungus

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Termite-egg Mimicry by a Sclerotium-Forming Fungus

Kenji Matsuura. Proc Biol Sci.

Abstract

Mimicry has evolved in a wide range of organisms and encompasses diverse tactics for defence, foraging, pollination and social parasitism. Here, I report an extraordinary case of egg mimicry by a fungus, whereby the fungus gains competitor-free habitat in termite nests. Brown fungal balls, called 'termite balls', are frequently found in egg piles of Reticulitermes termites. Phylogenetic analysis illustrated that termite-ball fungi isolated from different hosts (Reticulitermes speratus, Reticulitermes flavipes and Reticulitermes virginicus) were all very similar, with no significant molecular differences among host species or geographical locations. I found no significant effect of termite balls on egg survivorship. The termite-ball fungus rarely kills termite eggs in natural colonies. Even a termite species (Reticulitermes okinawanus) with no natural association with the fungus tended termite balls along with its eggs when it was experimentally provided with termite balls. Dummy-egg bioassays using glass beads showed that both morphological and chemical camouflage were necessary to induce tending by termites. Termites almost exclusively tended termite balls with diameters that exactly matched their egg size. Moreover, scanning electron microscopic observations revealed sophisticated mimicry of the smooth surface texture of eggs. These results provide clear evidence that this interaction is beneficial only for the fungus, i.e. termite balls parasitically mimic termite eggs.

Figures

Figure 1
Figure 1
Termite eggs and termite balls. (a) A pile of eggs in the nest of Reticulitermes virginicus. Termite eggs are transparent and oval, whereas termite balls (egg-mimicking fungal sclerotia) are brown and spherical. (b) Comparison of the shapes and colours of termite balls and termite eggs. Most termite balls are spherical, with rare occurrences of oval balls resulting from the fusion of two termite balls.
Figure 2
Figure 2
Phylogenetic position of the termite-ball fungi (TB) isolated from Reticulitermes speratus in Japan and from R. flavipes and R. virginicus in the USA based on nucleotide sequences of the ITS regions. Strict consensus of the 10 most parsimonious trees is shown. Bootstrap values are indicated for nodes having more than 50% support (500 replicates). GenBank accession numbers are shown in parentheses. The DNA sequence of the egg-pathogenic fungus isolated from dead eggs was identical to that of the termite-ball fungus isolated from the same colony (TB a1Rf).
Figure 3
Figure 3
Comparison of the piling rates of termite eggs, termite balls and dummy eggs (glass beads). Glass beads (0.2, 0.4 or 0.6 mm in diameter) that were coated (c) or not coated (nc) with egg chemicals were used as dummy eggs. For example, 0.2-c and 0.2-nc indicate 0.2 mm glass beads that were and were not coated with egg chemicals, respectively. Termite balls collected from egg piles were carried at the same rate as were termite eggs (Mann–Whitney U-test, Z=0.72, p=0.382). Different letters indicate significant differences at the 0.05 level, as shown by post hoc Scheffé's tests. Note that 0.4 mm beads are within the range of the short diameter of termite eggs.
Figure 4
Figure 4
Comparison of the frequency distributions of the short diameter of eggs, the diameter of termite balls collected from egg piles of each colony (accepted TBs) and the diameter of termite balls produced by fungi isolated from each colony (produced TBs). The data of two representative colonies (AA-A and BH-B) and the pooled data for all colonies are shown. Termites almost exclusively accepted only termite balls with diameters similar to those of eggs.
Figure 5
Figure 5
(a, b) Comparative observations of the micro-structure of the surfaces of an egg of R. flavipes, (c, d) a termite ball and (e, f) a sclerotium of the closely related corticioid fungus Athelia epiphylla, using a variable-pressure scanning electron microscope. Termite balls have remarkably smooth surfaces compared to those of the sclerotia of A. epiphylla. Note that this termite ball was formed on an agar plate without termites; therefore, the smooth surface structure is not the result of grooming by termites.

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