Phoretic nest parasites use sexual deception to obtain transport to their host's nest

Abstract

Cooperative behaviors are common among social insects such as bees, wasps, ants, and termites, but they have not been reported from insect species that use aggressive mimicry to manipulate and exploit prey or hosts. Here we show that larval aggregations of the blister beetle Meloe franciscanus, which parasitize nests of the solitary bee Habropoda pallida, cooperate to exploit the sexual communication system of their hosts by producing a chemical cue that mimics the sex pheromone of the female bee. Male bees are lured to larval aggregations, and upon contact (pseudocopulation) the beetle larvae attach to the male bees. The larvae transfer to female bees during mating and subsequently are transported to the nests of their hosts. To mimic the chemical and visual signals of female bees effectively, the parasite larvae must cooperate, emphasizing the adaptive value of cooperation between larvae. The aggressive chemical mimicry by the beetle larvae and their subsequent transport to their hosts' nests by the hosts themselves provide an efficient solution to the problem of locating a critical but scarce resource in a harsh environment.

Fig. 1.

Three steps in the Habropoda–Meloe aggressive mimicry system. (A) A typical aggregation of M. franciscanus triungulins on a grass blade. Aggregations average 6.9 ± 2.8 mm in diameter (range, 2–15 mm; mode = 10; n = 153). Of 153 triungulin aggregations measured, 55% were ≥7 mm. (B) A male H. pallida bee inspecting an M. franciscanus triungulin aggregation on the branch tip of the dune plant A. lentiginosus var. borreganus. (C) A male bee covered with M. franciscanus triungulin larvae on the dorsum.

Fig. 2.

Results of bioassays to characterize the nature of male bee attraction to triungulin aggregations or female bees. (A) Male bee inspection visits of triungulin aggregations, visual models of aggregations, and models treated with extracts of triungulins (n = 3) (χ² = 1.53, P = 0.22). Visual models received no visits and were not included in the data analysis. (B) Inspection visits of male bees to caged female bees, caged male bees, and empty cage controls (n = 9). Two-way ANOVA: treatment, F = 27.45, P = 0.0001, df = 2,17; trial, F = 1.63, P = 0.024, df = 5,17. Bars marked by different letters are significantly different (Student–Newman–Keuls procedure, P < 0.05).

Fig. 3.

Composition of extracts (mean percentages ± SD) from male (n = 12) and female (n = 14) bee heads and whole-body extracts of triungulin aggregations (n = 6). Numbers indicate hydrocarbon chain length, alkenes are indicated by Δ, and methyl branches are indicated with a numerical prefix. HC 22.55 and HC 22.65 were two unidentified hydrocarbons.

Fig. 4.

Positional isomeric composition (mean percentages ± SD) of the alkene fractions of the extracts of heads of male and female bees and of triungulin aggregations. Trace amounts of (Z)-9-C₂₁ and (Z)-11-C₂₁ also were detected in two of the six triungulin extracts.

Fig. 5.

Attraction of male bees to hydrocarbon blends mimicking fractions of an extract of a triungulin mass. “Unsat HC” treatment consisted of (Z)-9-C₂₁ (0.025 mg), (Z)-9-C₂₃ (0.860 mg), (Z)-11-C₂₁ (0.100 mg), (Z)-9-C₂₅ (1.25 mg), and (Z)-11-C₂₅ (0.252 mg); “Sat HC” treatment consisted of C₂₁ (0.089 mg), C₂₃ (1 mg), C₂₅ (0.252 mg), and C₂₇ (0.704 mg); “Total” treatment consisted of Unsat HC plus Sat HC (n = 5). Two-way ANOVA: treatment, F = 20.37, P = 0.0007, df = 2,14; trial, F = 4.01, P = 0.045, df = 4,14. Bars marked by the same letter are not significantly different (Student–Newman–Keuls procedure, P = 0.05).

Fig. 6.

Attraction of male bees to hydrocarbon blends mimicking the alkene fractions of female bees, male bees, and triungulins as determined from analyses of Figs. 3 and 4 and a solvent control (n = 12). Two-way ANOVA: treatment, F = 21.28, P < 0.0001, df = 3,47; trial, F = 1.61, P = 0.14, df = 11,47. Bars marked by the same letter are not significantly different (Student–Newman–Keuls procedure, α = 0.05). “Females” treatment consisted of (Z)-9-C₂₁ (0.090 mg), (Z)-9-C₂₃ (0.340 mg), (Z)-10-C₂₃ (0.145 mg), (Z)-11-C₂₃ (0.390 mg), (Z)-9-C₂₅ (0.500 mg), (Z)-10-C₂₅ (0.270 mg), (Z)-11-C₂₅ (0.150 mg), (Z)-12-C₂₅ (0.880 mg), (Z)-12-C₂₇ (0.315 mg), (Z)-13-C₂₇ (0.205 mg), (Z)-14-C₂₉ (0.160 mg), (Z)-9-C₃₁ (0.140 mg), and (Z)-15-C₃₁ (0.310 mg). “Males” treatment consisted of (Z)-9-C₂₃ (0.438 mg), (Z)-9-C₂₅ (0.500 mg), and (Z)-9-C₃₁ (0.234 mg). “Triungulin” treatment consisted of (Z)-9-C₂₃ (0.305 mg), (Z)-11-C₂₃ (0.068 mg), (Z)-9-C₂₅ (0.500 mg), and (Z)-11-C₂₅ (0.143 mg). Control treatment consisted of 50 μl of hexane.