Transgenerational effects of herbivory in a group of long‐lived tree species: maternal damage reduces offspring allocation to resistance traits, but not growth

Abstract

Summary Numerous studies have explored plant strategies of resource allocation to growth and/or resistance traits within a single generation. In contrast, exceedingly little is known about whether such patterns hold across generations; that is, in seedlings of plants that experienced maternal herbivory. In a common garden study with clonally replicated genotypes of three cottonwood taxa (Populus angustifolia, Populus fremontii and their F1 hybrids), we examined transgenerational response to maternal herbivory in terms of half‐sibling seedling offspring (i) germination and growth and (ii) constitutive vs. transgenerational plastic allocation to resistance (measured as both phytochemical content and concentration). Two major results emerged. First, we found that taxa (and often genotypes within a taxon) significantly differed in their constitutive allocation to both growth and resistance. Fremont (P. fremontii) seedlings grew up to seven times more rapidly than did narrowleaf (P. angustifolia) seedlings and had higher or similar content of two key phytochemical resistance traits. Overall, this led to a dilution effect in Fremont relative to narrowleaf, whereby concentrations of two key phytochemical resistance traits were more than 50% lower. Secondly, maternal herbivory by cottonwood leaf beetle larvae on foliage adjacent to developing seeds did not significantly alter offspring growth, but did decrease offspring phytochemical content by 10–55% relative to offspring of maternal control (undamaged) trees. As a result, concentrations of offspring phytochemical resistance traits were reduced by 10–18% in seedlings with maternal herbivory, relative to maternal control seedlings, across all three taxa. These patterns suggest an allocational trade‐off, whereby maternal damage results in maintenance of offspring seed size and growth traits at the expense of phytochemical defences in the next generation. Synthesis: This is the first instance in which transgenerational effects of herbivory on growth and defence traits have been described in long‐lived, woody plant species. Populus differs substantially from herbaceous plant species or short‐lived animals in which transgenerational plasticity of resistance has been examined, in terms of life history (time from germination or hatching to reproductive maturity) and/or in the lag time between generations. These differences may influence the ecological and evolutionary relevance of transgenerational plasticity in defence.