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Conserved Class of Queen Pheromones Stops Social Insect Workers from Reproducing

Science  17 Jan 2014:
Vol. 343, Issue 6168, pp. 287-290
DOI: 10.1126/science.1244899

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  1. Fig. 1 Queen pheromone bioassays.

    The results demonstrate that long-chain cuticular hydrocarbons act as a conserved class of sterility-inducing queen pheromones in three independently evolved social insect lineages, represented by the wasp V. vulgaris (A), the bumblebee B. terrestris (B), and the ant C. iberica (C). Treatment of queenless worker groups with the linear alkanes n-C27 and n-C29 and the methyl alkane 3-MeC29 caused a two- to sevenfold reduction in the odds of workers having fully developed ovaries in the common wasp and the Iberian ant (bar charts, red bars) relative to a pentane-treated control (left, stacked bar charts) (significance levels based on binomial mixed models: *P < 0.05, **P < 0.01, and ***P < 0.001; see table S2 for detailed statistics). Furthermore, the probability of workers having regressed ovaries (blue bars) was increased ~two- to four-fold by treating colonies with n-C27, n-C28, n-C29, and 3-MeC29 in the common wasp, n-C25 in the bumblebee, and n-C27 and 3-MeC29 in the Iberian ant. Decreased worker ovary development mimicked the effect of the presence of a live queen, as did the increased worker ovary regression observed in the bumblebee (table S2). By contrast, none of four queen-specific esters tested (E1 to E4: eicosyl, docosyl, tetracosyl, and hexacosyl oleate) significantly influenced worker ovary development in the bumblebee. Colony size and the number of males present were included in the model whenever they had a significant effect (table S2).

  2. Fig. 2 The evolutionary history of queen and fertility signals across major clades of social hymenopteran insects.

    Each alternately shaded clade indicates an independent origin of eusociality (12). The pie charts show the likelihoods of different compound classes being used as queen or fertility signals as inferred from a maximum likelihood ancestral state reconstruction under a single-rate evolutionary model. Saturated hydrocarbons (linear and methyl-branched alkanes) receive very high support for being used as conserved queen or fertility signals across several independent origins of eusociality (red pie charts, see likelihood values in table S5; branches with likelihood of >50% are highlighted in red). By contrast, the use of other compound classes, such as the keto acid (E)-9-oxo-2-decenoic acid (2) (dark green) and the esters ethyl palmitate and methyl linoleate (19) in A. mellifera honeybees (yellow) or the alkene (Z)-9-nonacosene in Odontomachus ants (9) (blue), appear to be either derived or highly taxon-specific (pie charts of maximum likelihood reconstructions of particular compound classes are shown when likelihood values are >50%). Data are based either on the overrepresentation of particular compound classes on queens relative to workers or on direct experimental evidence for specific pheromones being used to suppress worker reproduction (solid highlights indicate direct physiological inhibition; open boxes indicate aggression-mediated inhibition) (table S3). Species tested in the present study are marked with arrows. The main active compounds are shown in the insets (A) V. vulgaris and (D) C. iberica: a = heptacosane, b = nonacosane, c = 3-methylnonacosane. (B) A. mellifera: d = (E)-9-oxo-2-decenoic acid, e = ethyl palmitate, f = (E)-β-ocimene, g = methyl linoleate. (C) B. terrestris: h = pentacosane. (E) L. flavus and (F) L. niger: i = 3-methylhentriacontane.