Bumblebees mediate landscape effects on a forest herb's population genetic structure in European agricultural landscapes

Spatially isolated plant populations in agricultural landscapes exhibit genetic responses not only to habitat fragmentation per se but also to the composition of the landscape matrix between habitat patches. These responses can only be understood by examining how the landscape matrix influences among-habitat movements of pollinators and seed vectors, which act as genetic linkers among populations. We studied the forest herb Polygonatum multiflorum and its associated pollinator and genetic linker, the bumblebee Bombus pascuorum, in three European agricultural landscapes. We aimed to identify which landscape features affect the movement activity of B. pascuorum between forest patches and to assess the relative importance of these features in explaining the forest herb's population genetic structure. We applied microsatellite markers to estimate the movement activity of the bumblebee as well as the population genetic structure of the forest herb. We modelled the movement activity as a function of various landscape metrics. Those metrics found to explain the movement activity best were then used to explain the population genetic structure of the forest herb. The bumblebee movement activity was affected by the cover of maize fields and semi-natural grasslands on a larger spatial scale and by landscape heterogeneity on a smaller spatial scale. For some measures of the forest herb's population genetic structure, that is, allelic richness, observed heterozygosity and the F-value, the combinations of landscape metrics, which explained the linker movement activity best, yielded lower AICc values than 95% of the models including all possible combinations of landscape metrics.Synthesis: The genetic linker, B. pascuorum, mediates landscape effects on the population genetic structure of the forest herb P. multiflorum. Our study indicates, that the movement of the genetic linker among forest patches, and thus the pollen driven gene flow of the herb, depends on the relative value of floral resources in the specific landscape setting. Noteworthy, the population genetic structure of the long-lived, clonal forest herb species correlated with recent land-use types such as maize, which have been existing for not more than a few decades within these landscapes. This underscores the short time in which land-use changes can influence the evolutionary potential of long-lived wild plants. Bumblebees can connect isolated populations of forest herbs within agricultural landscapes by moving between forest patches. These movements are influenced by specific aspects of the landscape. These same landscape aspects also partly explain the population genetic structure of a forest herb species associated with bumblebees as pollinators.image