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.

Limited effects of population age on the genetic structure of spatially isolated forest herb populations in temperate Europe.

Due to multiple land-cover changes, forest herb populations residing in forest patches embedded in agricultural landscapes display different ages and, thus, experience differences in genetic exchange, mutation accumulation and genetic drift. The extent of divergence in present-day population genetic structure among these populations of different ages remains unclear, considering their diverse breeding systems and associated pollinators. Answering this question is essential to understand these species' persistence, maintenance of evolutionary potential and adaptability to changing environments. We applied a multi-landscape setup to compare the genetic structure of forest herb populations across forest patches of different ages (18-338 years). We studied the impact on three common slow-colonizer herb species with distinct breeding systems and associated pollinators: Polygonatum multiflorum (outcrossing, long-distance pollinators), Anemone nemorosa (outcrossing, short-distance pollinators) and Oxalis acetosella (mixed breeding). We aimed to assess if in general older populations displayed higher genetic diversity and lower differentiation than younger ones. We also anticipated that P. multiflorum would show the smallest while O. acetosella the largest difference, between old and young populations. We found that older populations had a higher observed heterozygosity (H o) but a similar level of allelic richness (A r) and expected heterozygosity (H e) as younger populations, except for A. nemorosa, which exhibited higher A r and H e in younger populations. As populations aged, their pairwise genetic differentiation measured by D PS decreased independent of species identity while the other two genetic differentiation measures showed either comparable levels between old and young populations (G" ST) or inconsistency among three species (cGD). The age difference of the two populations did not explain their genetic differentiation. Synthesis: We found restricted evidence that forest herb populations with different ages differ in their genetic structure, indicating that populations of different ages can reach a similar genetic structure within decades and thus persist in the long term after habitat disturbance. Despite their distinct breeding systems and associated pollinators, the three studied species exhibited partly similar genetic patterns, suggesting that their common characteristics, such as being slow colonizers or their ability to propagate vegetatively, are important in determining their long-term response to land-cover change.

Context matters: the landscape matrix determines the population genetic structure of temperate forest herbs across Europe.

Context: Plant populations in agricultural landscapes are mostly fragmented and their functional connectivity often depends on seed and pollen dispersal by animals. However, little is known about how the interactions of seed and pollen dispersers with the agricultural matrix translate into gene flow among plant populations. Objectives: We aimed to identify effects of the landscape structure on the genetic diversity within, and the genetic differentiation among, spatially isolated populations of three temperate forest herbs. We asked, whether different arable crops have different effects, and whether the orientation of linear landscape elements relative to the gene dispersal direction matters. Methods: We analysed the species' population genetic structures in seven agricultural landscapes across temperate Europe using microsatellite markers. These were modelled as a function of landscape composition and configuration, which we quantified in buffer zones around, and in rectangular landscape strips between, plant populations. Results: Landscape effects were diverse and often contrasting between species, reflecting their association with different pollen- or seed dispersal vectors. Differentiating crop types rather than lumping them together yielded higher proportions of explained variation. Some linear landscape elements had both a channelling and hampering effect on gene flow, depending on their orientation. Conclusions: Landscape structure is a more important determinant of the species' population genetic structure than habitat loss and fragmentation per se. Landscape planning with the aim to enhance the functional connectivity among spatially isolated plant populations should consider that even species of the same ecological guild might show distinct responses to the landscape structure. Supplementary Information: The online version contains supplementary material available at 10.1007/s10980-021-01376-7.