The extended consequences of genetic conductivity: Mating distance affects community phenotypes in Norway spruce

Anthropogenic landscape-level alterations such as habitat fragmentation and long distance translocation of genetic material are currently altering the genetic connectivity and structure of forest tree populations globally. As the susceptibility of individual trees to dependent organisms is often genetically determined, it is possible that these genetic changes may extend beyond individuals to affect associated communities. To test this, we examined how variation in crossing distance among the progeny of 18 controlled crosses of Norway spruce (Picea abies) populations occurring across central Sweden affected chemical defense, and subsequently, a small community of galling Adelges aphids infecting planted trees at two common garden trails. Although crossing distance did not influence growth, vitality or reproduction in the studied population, it did influence the expression of one candidate defensive chemical compound, apigenin, which was found in higher concentrations within outcrossed trees. We also show that this variation in apigenin induced by crossing distance correlated with susceptibility to one member of the galling community but not the other. Furthermore, the effect of crossing distance on galling communities and the general susceptibility of Norway spruce to infection also varied with environment. Specifically, in the more benign environment, inbred trees suffered greater gall infection than outcrossed trees, which is contrary to general predictions that the effects of inbreeding should be more pronounced in harsher environments. These findings suggest that the effects of variation in crossing distance in forest trees can extend beyond the individual to influence whole communities.