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. 2010 Jul 20;107(29):12963-8.
doi: 10.1073/pnas.1004675107. Epub 2010 Jul 6.

Identification of a pheromone regulating caste differentiation in termites

Kenji Matsuura  1 , Chihiro Himuro, Tomoyuki Yokoi, Yuuka Yamamoto, Edward L Vargo, Laurent Keller
Affiliations

Identification of a pheromone regulating caste differentiation in termites

Kenji Matsuura et al. Proc Natl Acad Sci U S A. .

Abstract

The hallmark of social insects is their caste system: reproduction is primarily monopolized by queens, whereas workers specialize in the other tasks required for colony growth and survival. Pheromones produced by reigning queens have long been believed to be the prime factor inhibiting the differentiation of new reproductive individuals. However, there has been very little progress in the chemical identification of such inhibitory pheromones. Here we report the identification of a volatile inhibitory pheromone produced by female neotenics (secondary queens) that acts directly on target individuals to suppress the differentiation of new female neotenics and identify n-butyl-n-butyrate and 2-methyl-1-butanol as the active components of the inhibitory pheromone. An artificial pheromone blend consisting of these two compounds had a strong inhibitory effect similar to live neotenics. Surprisingly, the same two volatiles are also emitted by eggs, playing a role both as an attractant to workers and an inhibitor of reproductive differentiation. This dual production of an inhibitory pheromone by female reproductives and eggs probably reflects the recruitment of an attractant pheromone as an inhibitory pheromone and may provide a mechanism ensuring honest signaling of reproductive status with a tight coupling between fertility and inhibitory power. Identification of a volatile pheromone regulating caste differentiation in a termite provides insights into the functioning of social insect colonies and opens important avenues for elucidating the developmental pathways leading to reproductive and nonreproductive castes.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Female neotenics and eggs suppress the differentiation of new female neotenics. (A) Termite royals with workers and brood. Female neotenics (FN) are indicated by arrowheads. (B) Presence of current FN significantly suppressed the differentiation of new female (nympoid) reproductives from nymphs in comparison with controls (P < 0.001, Tukey's HSD). Removal of eggs did not significantly reduce the inhibitory effect (P = 0.42). (C) Presence of current functional neotenics significantly suppressed the differentiation of new female (ergatoid) reproductives from workers (P < 0.001, Tukey's HSD). Removal of eggs did not significantly reduce the inhibitory effect (P = 0.97). (D) Continuous addition of 100 eggs per day (Egg ++) suppressed the differentiation of new female neotenics from workers (P < 0.01), but 20 eggs per day (Egg +) did not have a significant effect compared with controls (P = 0.34). (E) Volatiles of current female neotenic reproductives through stainless steel mesh significantly suppressed the differentiation of new female neotenics from nymphs (P < 0.001). Values denote the mean ± SEM of five replications.
Fig. 2.
Fig. 2.
Headspace GC-MS analysis. (A) Chromatograms of headspace-collected volatiles of female neotenics, eggs, workers, and nymphs. Female neotenic and egg volatiles consisted of identical compounds, nBnB and 2M1B, whereas workers and nymphs did not have these compounds. STD, toluene as an internal standard. (B) Mass spectra of nBnB from female neotenics (Upper) and of commercial origin (Lower). (C) Mass spectra of 2M1B from female neotenics (Upper) and of commercial origin (Lower).
Fig. 3.
Fig. 3.
Suppression of the differentiation of new female neotenics by a blend of synthetic nBnB and 2M1B. (A) Experimental setup for the inhibitory bioassay of synthetic volatiles. (B) Inhibitory effect of an artificial pheromone blend. A 2:1 mixture of nBnB and 2M1B suppressed the differentiation of new female neotenics (P < 0.001, Tukey's HSD), whereas n-butyl acetate, an ester (control 2), did not (P = 0.82) compared with control 1 (distilled water). (C) Comparison of inhibitory effect of the individual compounds and a 2:1 mixture of nBnB and 2M1B. The blend significantly suppressed the differentiation of new female neotenics (P < 0.001, Tukey's HSD), whereas neither nBnB alone (P = 0.97) nor 2M1B alone (P = 0.99) had a significant effect compared with the control (distilled water). Values denote the mean ± SEM of five replications.
Fig. 4.
Fig. 4.
Role of egg volatiles as an attractant pheromone. (A) Addition of nBnB and 2M1B to TERP (consisting of lysozyme and β-glucosidase) significantly increased the rate at which dummy eggs were piled up. Dummy eggs coated only with nBnB and 2M1B were not carried into egg piles. Different letters indicate significant differences among treatments (P < 0.05, Tukey's HSD). (B) Proposed functions of nBnB and 2M1B from female reproductives and eggs. These volatiles serve as an attractant to locate eggs and female reproductive and also act to inhibit the differentiation of female neotenics from nymphs and workers. Values denote the mean ± SEM of 15 replications (five replications × three colonies).
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