Mechanisms and specifictiy of sequestration in the genus Athalia
Final Report Abstract
Sequestration of various plant metabolites was until now described in 250 insect species. However, little is known about specificities or metabolism of sequestered compounds. Larvae of the sawfly genus Athalia (Hymenoptera: Tenthredinidae) are specialised on different plant families. All here investigated species were found to sequester, i.e. take up and store, the characteristic glucosides from their host plants within the Brassicaceae or Plantaginaceae in their haemolymph. The Athalia species specialised on Brassicaceae, A. rosae, A. liberta and A. lugens, sequester glucosinolates, whereas the Plantaginaceae-feeding species A. cordata and A. circularis sequester iridoid glucosides. The main glucosides were furthermore carried through the pupal stage to the imagines. The metabolism of glucosinolates was investigated in A. rosae larvae using feeding experiments with (radiolabelled) benzylglucosinolate and screening for degradation metabolites by UHPLC-TOF-MS (ultra high performance liquid chromatography coupled to a time of flight mass spectrometer) with final characterisation by NMR. From the results the following scenario for the metabolic pathway of glucosinolates can be proposed: benzylglucosinolate is sequestered in the haemolymph, where it is degraded first to desulfobenzylglucosinolate, which is subsequently sulfated at the sugar moiety to desulfobenzylglucosinolate sulfate. This metabolite is then passed in the gut and excreted. Intact benzylglucosinolate entering the gut directly is sulfated to benzylglucosinolate sulfate and likewise excreted. Sulfotransferases must be thus present in both the haemolymph and the gut. This metabolism pathway is yet another way of dealing with glucosinolates that has not been described for any other insect species feeding on Brassicaceae so far. As species of the genus Athalia are specialised on host plants of different plant families, host plant shifts must have taken place during the evolution of this genus. Here we propose that the ancestral host plants were species of the Lamiales and the use of Brassicaceae is derived. This assumption is based on the finding, that all Brassicaceae-feeding species were able to sequester the iridoid glucoside catalpol in their haemolymph, whereas the Plantaginaceae-feeding species did not sequester the glucosinolate sinalbin in manipulation experiments. Furthermore, adults of all five species showed pharmacophagous behaviour on the neo-clerodane diterpenoid clerodendrin B, which occurs only in Lamiales. A larval association of a common ancestor with plants of the Lamiales, which harbour species that contain both iridoid glucosides and clerodendrins, would explain the observed patterns. The sequestered glucosides were tested for their effectiveness as anti-predator trait. Larvae of all investigated Athalia spp. show the phenomenon of “easy bleeding”. When predators with biting-chewing mandibles attack the larvae, the larval integument disrupts easily and haemolymph exudes. Haemolymph of both A. cordata and A. rosae efficiently deterred ant workers of Myrmica rubra, but haemolymph of A. cordata was more deterrent than that of A. rosae. This is likely due to higher glucoside concentrations present in the haemolymph of A. cordata, but may additionally be based on the fact that catalpol (iridoid glucoside) itself was more deterrent than sinalbin (glucosinolate). When larvae of A. rosae feed on flowers of Sinapis alba they develop faster and are fitter than larvae feeding on leaves. During their development, larvae move from the leaves to the flowers. It remains to be tested how general this phenomenon is. Overall, sawflies of the genus Athalia provide a unique and exemplary case in the field of chemical ecology as three different metabolite classes - glucosinolates, iridoid glucosides and neo-clerodane diterpenoids – are used to mediate different ecological interactions in this genus. The phytophagous sawflies of the genus Athalia have evolved and conserved complex dependencies on plant secondary metabolites, which they gained through feeding on various plant families.
Publications
- (2009) Plant chemistry and insect sequestration. Chemoecology 19, 117-154
Opitz S.E.W., Müller C.
- (2010) Folivory versus florivory – adaptiveness of flower-feeding. Naturwissenschaften 97, 79-88
Bandeili B., Müller C.
- (2010) Sequestration of glucosinolates and iridoid glucosides in sawfly species of the genus Athalia and their role in defence against ants. Journal of Chemical Ecology 36, 148-157
Opitz S.E.W., Jensen S.R. & Müller C.
