Multi-trait mimicry of ants by a parasitoid wasp

Many animals avoid attack from predators through toxicity or the emission of repellent chemicals. Defensive mimicry has evolved in many species to deceive shared predators, for instance through colouration and other morphological adaptations, but mimicry hardly ever seems to involve multi-trait similarities. Here we report on a wingless parasitoid wasp that exhibits a full spectrum of traits mimicing ants and affording protection against ground-dwelling predators (wolf spiders). In body size, morphology and movement Gelis agilis (Ichneumonidae) is highly similar to the black garden ant (Lasius niger) that shares the same habitat. When threatened, G. agilis also emits a volatile chemical that is similar to an ant-produced chemical that repels spiders. In bioassays with L. niger, G. agilis, G. areator, Cotesia glomerata and Drosophila melanogaster, ants and G. agilis were virtually immune to spider attack, in contrast the other species were not. Volatile characterisation with gas chromatography-mass spectrometry identified G. agilis emissions as 6-methyl-5-hepten-2-one, a known insect defence semiochemical that acts as an alarm pheromone in ants. We argue that multi-trait mimicry, as observed in G. agilis, might be much more common among animals than currently realized. M imicry is widespread amongst plants and animals and involves the resemblance of one species to another, at least to the benefit of the mimic 1-4. For instance, the Malaysian orchid mantis Hymenopus coronatus visually mimics flowers such that it attracts more pollinator prey than the flowers it resembles 5. To avoid attack from shared predators, prey species may also mimic morphological features of a co-existing unpalatable or toxic model species 3 , as has long been observed and studied in hoverflies, butterflies and snakes 2,6-9. In hoverflies, which visually resemble stinging bees or wasps, colour mimicry can coincide with behavioural mimicry, such as mock stinging, wing wagging and leg waving 10,11 or activity patterns 2. Predators and prey can also be deceived via chemical mimicry: some spiders attract their lepidopteran prey through the emission of moth sex pheromones 12 but chemical mimicry appears to be less frequently adopted as an anti-predator strategy 13-15. Whilst behavioural mimicry often coincides with morphological similarity, mimicry only rarely seems to require convergence of a greater number of traits 13,16 .The secondary hyperparasitoid Gelis agilis could represent an exception, as it shows several distinct similarities to sympatric ant species. Gelis agilis is a small (3-5 mm long) wingless, asexually reproducing parasitoid wasp that attacks several host species, including the pupae of other parasitoids 17,18. Adult G. agilis first paralyze the host with venom and then oviposit a single egg onto the exterior of the host's body 18. After hatching, the G. agilis larva feeds on the moribund host, eventually consuming all of it prior to pupation. Gelis agilis is extremely abundant in grassy habitats across much of Eurasia 18 and co-occurs and shares predators with several ant species. Its potential predators include wolf spiders, which are visually foraging diurnal hunters that attack a wide range of prey types on the ground 19,20. In morphology (body size, colour) and behaviour, G. agilis (Fig. 1a) closely resembles several species of ants that occur in the same habitat, including the common black garden ant, Lasius niger (Fig. 1b). Moreover, when alarmed the parasitoid releases a pungent and distinctive odour. Here, we test the hypotheses that ant-mimicry by G. agilis acts as a defensive strategy to reduce attack by wolf spiders and that chemical mimicry is facilitated by the emission of an ant-like alarm pheromone 21 .