Reduced seed viability in exchange for transgenerational plant protection in an endophyte-symbiotic grass: does the defensive mutualism concept pass the fitness test?

Abstract

Abstract Background and Aims Epichloë endophytes are vertically transmitted via grass seeds and chemically defend their hosts against herbivory. Endophyte-conferred plant defence via alkaloid biosynthesis might occur independently of costs for host plant growth. However, fitness consequences of endophyte-conferred defence and transgenerational effects on herbivore resistance of progeny plants are rarely studied. The aim of this study was to test whether severe defoliation in mother plants affects their seed production, seed germination rate and the endophyte-conferred resistance of progeny plants. Methods In a field study, we tested the effects of defoliation and endophyte symbiosis (Epichloë uncinata) on host plant (Festuca pratensis) performance, loline alkaloid concentrations in leaves and seeds, seed biomass and seed germination rates. In a subsequent greenhouse study, we challenged the progeny of the plants from the field study to aphid herbivory and tested whether defoliation of mother plants affects endophyte-conferred resistance against aphids in progeny plants. Key Results Defoliation of the mother plants resulted in a reduction of alkaloid concentrations in leaves and elevated the alkaloid concentrations in seeds when compared with non-defoliated endophyte-symbiotic plants. Viability and germination rate of seeds of defoliated endophyte-symbiotic plants were significantly lower compared with those of non-defoliated endophyte-symbiotic plants and endophyte-free (defoliated and non-defoliated) plants. During 6 weeks of growth, seedlings of defoliated endophyte-symbiotic mother plants had elevated alkaloid concentrations, which was negatively correlated with aphid performance. Conclusions Endophyte-conferred investment in higher alkaloid levels in seeds, elicited by defoliation, provided protection from herbivores in progenies during the first weeks of plant establishment. Better protection of seeds via high alkaloid concentrations was negatively correlated with seed germination, indicating a trade-off between protection and viability.