Loss of heterosis and family-dependent inbreeding depression in plant performance and resistance against multiple herbivores under drought stress

1. Inbreeding depression (ID), outbreeding depression (OD) and heterosis can occur concurrently in plant populations. ID often increases under environmental stress, but the combined effects of inbreeding, outbreeding between populations and environmental stress, such as drought, on plant performance and herbivore resistance remain unclear. 2. In order to determine environment-dependent and family-dependent ID, OD and heterosis, we conducted a common garden experiment with plants from five populations of Brassica nigra. Inbred, within-population outbred and between-population outbred plant families were exposed to drought or ambient water levels. We recorded the abundance and damage caused by specialist herbivores from contrasting feeding guilds, that is the phloem-feeding Brevicoryne brassicae, the leaf-chewing Psylliodes chrysocephalus and the stem-boring Ceutorhynchus quadridens larvae. 3. Drought stress had negative effects on growth, herbivore resistance and resistance against B. brassicae and positive effects on investments in reproductive output and plant secondary metabolites (sinigrin). We found drought stress-induced loss of heterosis for plant height and investment in reproductive output. Between-population outbred plants were more sensitive to drought stress in terms of above-ground biomass compared to within-population outbred plants. 4. Drought and inbreeding synergistically negatively influenced traits related to growth and reproductive output (environment-dependent inbreeding depression, EDID). There was high variation among families within populations in the degree of ID and EDID. Genetic variation in EDID could buffer the negative effects of genetic stress associated with habitat fragmentation and concurrent environmental stress. In order to capture fully the effects of both inbreeding and between-population outbreeding under stress, the different spatial scales of the effects of inbreeding and between-population outbreeding should be taken into account. 5. Synthesis. Our results indicate that drought stress influences not only inbreeding depression (ID), but also heterosis. These findings shed new light on the combined effects of anthropogenic environmental change and the genetic consequences of habitat fragmentation on plants and their interactions with other organisms. Conservation programmes aiming to restore genetically degraded populations with the translocation of individuals between populations should consider environmental stress as a risk factor.