Chemical ecology of a solitary wasp

Project leader: Erhard Strohm

Staff: Gudrun Herzner, Thomas Schmitt, Susanne Bordon, Silke Fregin, Claudia Laurien-Kehnen, Johannes Kroiss, Corinna Pohl

Objectives: We are generally interested in the evolutionary and ecological aspects of chemical communication and interaction with parasites and competitors that is mediated by chemical compounds.

Communication between conspecifics plays an important role in particular for mate finding and mate choice. However, how such signals evolve is not well understood. This is particularly true for chemical signals that are probably the most important kind of signals at least among insects. The sensory drive theory states that males should use courtship signals that either attract females or for which females have a high sensitivity. The high sensitivity in females is assumed to be the result of selection for certain cues in a non mating context e.g. foraging. Males incorporate such cues in their courtship signals and are therefore more attractive or more conspicuous. We investigate the pheromone communication in a solitary sphecid wasp, the European beewolf (Philanthus triangulum, Hymenoptera, Sphecidae) to test the sensory drive theory. Females of this species are highly specialized hunters of honeybees and males establish and scent mark mating territories.

The second major part of our studies on the chemical ecology of beewolves is the interaction with brood parasites. We investigate the interaction with a specialised cuckoo wasp whose larvae kill the beewolf larvae. We are interested in protective strategies employed by the females (temporal and spatial evasion, behavioural adaptations) as well as counterstrategies of the parasites (camouflage). Furthermore, we are interested in the mechanisms of the action of protective compounds against fungi that grow on the paralysed honeybees and destroy the larval provisions.

Approach: Sensory drive: It was already known that a long chained alcohol, Z-(11)-eicosenol occurs in the alarm pheromone of honeybees as well as in the sex pheromone of male European beewolves. We proposed and tested a three step scenario for the evolution of the sex pheromone in beewolves. First, honeybees (the only prey of the females) smell of eicosenol. Second, females use eicosenol to locate or identify honeybees and have,therefore, evolved a high sensitivity for this substance. Third, due to this female sensitivity for eicosenol, males incorporated it in their pheromone to be more conspicuous or more attractive for females. We use a combination of chemical analyses (gas-chromatography, mass spectrometry, FTIR, enantioselective GC, derivatisations) and behavioural bioassays to test our predictions.

Host-parasite interaction: We observe interactions between beewolf females and cuckoo wasps and analyse the cuticular hydrocarbons to assess whether cuckoo wasps are chemically camouflaged (GC-MS). The investigations of the beewolf-fungus interaction mainly consist of microbiological bioassays and chemical analyses (GC-MS).

Progress:

Sensory drive: First, we could prove the occurrence of eicosenol on the cuticle of honeybees, which was hitherto not known. We were even able to show that eicosenol is present in the air surrounding foraging honeybees. Thus, the first prediction of our scenario is met. Second, we showed that beewolf females use olfactory cues to identify honeybees and to elicit attacks. Most interestingly, eicosenol was a necessary component to elicit attacks. Thus, the second prediction of our scenario is met as well. It is remarkable that very small amounts of eicosenol are behaviourally effective, confirming a very high sensitivity of beewolf females for this substance. Third, we reanalyzed the pheromone of male Euroepan beewolves. Besides eicosenol we found another 7 components that are also present on the cuticle of honeybees, only 3 compounds were not present on honeybees. Thus, the similarity between the male pheromone and the odour of foraging honeybees is much greater than expected, supporting the third prediction, that males mimic the chemical cues of the females' prey at least partly. Altogether our results provide strong evidence for a role of sensory drive in the evolution of a sex pheromone.

Host-parasite interaction: Our results indicate that beewolf females might escape parasitism by being active late in the evening. Furthermore, beewolf females are able to detect the presence of cuckoo wasps and respond by removing parasitized bees. The highly specialised cuckoo wasps, in turn, have evolved chemical mimicry to avoid detection in the nests of their hosts. This sets the stage for a coevolutionary arms race between host and parasite. Beewolf females have also evolved adaptations to deal with fungi that grow on the paralysed bees. They lick the whole surface of their prey and apply a secretion from a postpharyngeal gland (the existence of which is in itself interesting since this kind of gland otherwise occurs only in ants). The major effect of this secretion is, however, not mediated by its chemical activity but by changing the microclimate on the prey items, i.e. a physical effect: The secretion prevents water condensation and, thus, deteriorates the growth conditions for fungi.

Significance: The sensory drive theory has received convincing support from model species that exhibit acoustic or visual courtship cues. However, this study is to our knowledge the first that tests the whole scenario of the evolution of a chemical signal. Furthermore, our study shows that a very minor component of an odour (like the eicosenol on honeybees) can have a crucial biological significance. Similarly, despite the commonness of chemical cues as courtship signals surprisingly little is known about their role for female choice. This is probably the result of difficulties in dealing with chemical signals since these are mostly only available in minor amounts. One advantage of our model system is that male beewolves produce large amounts of pheromone and we have non invasive methods to analyse it. Thus, we have the opportunity to investigate a phenomenon that is not accessible in most study species.

Chemical mimicry has been shown in a number of cases for nest parasites of social species such as ants and is mostly accomplished by the sequestration of chemicals from members of the host nest. However, real chemical mimicry in a brood parasite of a solitary species as is probably the case in our beewolf/cuckoo wasp system has not been reported before. The described physical effect of prey conservation by preventing water condensation on the prey is, to our knowledge, new to biology and provides promising aspects for a technical application.

Future projects: We are going to assess whether the male pheromone varies between distant populations and to test whether females choose males with regard to the population, to their size (age), or relatedness. We are also trying to investigate the neuro-physiological basis of female choice by use of electro-antennal detection and calcium imaging techniques. This might provide exceptionally interesting insights in the physiology of a complex olfactory cue that has an important biological significance.

With regard to the host-parasite interaction, we are currently mainly interested in the coevolutionary interaction between the European beewolf and the specialised cuckoo wasp. We will test whether there is a covariation between host and parasite across widely separated populations with regard to their cuticular hydrocarbons.

Collaborations: Peter Schreier, Frank Heckel (Food Chemistry, Würzburg University), Torsten Meiners, Joachim Ruther (Animal Ecology, Free University Berlin), Carlo Bicchi (Pharmacy, Turin University), Gerhard Krammer (Symrise AG, Holzminden), Gudrun Herzner, Christoph Kleineidam, Wolfgang Rössler (Animal Physiology and Sociobiology, Würzburg University), Wilhelm Boland (MPI, Jena), Klaus Pescke (Zooloy Freiburg University).

Publications:

In preparation:

• Herzner G, Schmitt T, Schreier P, Strohm E (submitted) Brothers smell similar: a family effect in the composition of the sex pheromone of male European beewolves (Hymenoptera, Sphecidae)
• Herzner G, Schmitt T, Schreier P, Strohm E (in prep.) Fungus growth on the honeybee prey is delayed by a reduction of water condensation by the postpharyngeal secretion of female European beewolves (Hymenoptera, Sphecidae)
• Rybak J, Groh C, Strohm E, Tautz J (in prep.) Brain anatomy of the European beewolf, Philanthus triangulum. A morphometric and 3D-reconstruction study.
• Schmitt T, Herzner G, Schreier P, Strohm E (in prep.) How to attract females: Sensory exploitation and the sex pheromone of male European beewolves (Hymenoptera, Sphecidae)
• Strohm E, Schmitt T, Herzner G, Laurien-Kehnen C, Boland W, Schreier P (in prep.) Cuckoos in wolves' clothing? Chemical mimicry in a specialised cuckoo wasp of the European beewolf (Hymenoptera, Chrysididae and Sphecidae).
• Strohm E (in prep.) How can cleptoparasitic drosophilid flies emerge from nests of the Red Mason Bee?
• Strohm E, Schmitt T, Herzner G, Peschke K, Boland W, Schreier P (in prep.) Morphology and chemistry of the postpharyngeal gland in female European beewolves (Hymenoptera, Sphecidae).

Current external funding: DFG: SFB 554 TP B3.

Beewolf female flying to its nest with a paralysed honeybee (by G. Herzner)