Pollinator functional group abundance and floral heterogeneity in an agroecological context affect mating patterns in a self-incompatible wild plant

Premise: Restoration of semi-natural field margins can elevate pollinator activity. How they support wild plant gene flow through interactions between pollinators and spatio-temporal gradients in floral resources remains largely unknown. 

Methods: Using a farm-scale experiment, we tested how mating outcomes (expected heterozygosity and paternity correlation) of the wild, self-incompatible plant Cyanus segetum transplanted into field margins (sown wildflower or grass-legume strips) were affected by the abundance of different pollinator functional groups (defined by species traits). We also investigated how the maternal plant attractiveness, conspecific pollen donor density and heterospecific floral richness and density interacted with pollinator functional group abundance to modulate C. segetum mating outcomes.

Key Results: Multiple paternity increased (=lower paternity correlation) with greater local abundance of hoverflies (syrphids) and female medium-sized wild bees (albeit the latter’s effect diminished with decreasing maternal plant attractiveness), and the presence of male bumblebees (Bombus) under low local floral richness. Cyanus segetum progeny genetic diversity increased with male Bombus presence but decreased with greater abundance of syrphids and honeybees (Apis mellifera).

Conclusions: Overall, field margins supported plant-pollinator interactions ensuring multiple paternity and conservation of allelic diversity in C. segetum progeny. The contribution to plant mating outcomes of different pollinator functional groups was dictated by their local abundance or specific floral preferences (i.e. male Bombus). The local floral richness or maternal plant attractiveness sometimes modulated these relationships. This complex response of wild plant mating patterns to community interactions has implications for the use of field margins to restore functional pollination systems in farmed landscapes.

Methods
The data were collected in May-July 2019 on a farm-scale agroecological experiment (INRAE CA-SYS platform) in Burgundy, France (47°19'06.7"N 5°04'17.6"E), with the aim of investigating how the abundance of different pollinator functional groups (defined by species traits) interacted with the local floral context (maternal plant attractiveness, conspecific pollen donor density, heterospecific floral richness and density) to modulate the mating outcomes (expected heterozygosity, multilocus paternity correlation) of the wild, self-incompatible plant Cyanus segetum transplanted in field margins (wildflower strips or grass-legume strips).                        

144 focal C. segetum plants originating from seeds obtained from ARBIOTECH (Saint-Gilles, France) were germinated in controlled conditions before being transplanted at the rosette stage in 16 agroecological infrastructures (field margins) across the farm (10 wildflower strips and 6 grass/legume strips). Each focal plant plot consisted of three triplets of focal C. segetum, for a total of nine focal plants per plot.                        

From May to July 2019, we monthly monitored the reproductive development of the focal C. segetum plants and the local floral assemblage of the field margin (6 quadrats of 2 m x 50 cm along a transect of 100 m x 2 m centered on the focal plot; n = 16 transects).                                         

We also conducted bimonthly surveys of plant-pollinator interactions with the focal plants (plot-scale surveys, 15 minutes, n = 16 plots) and in the multispecies plant assemblage of the field margins (15 minutes of slow walk along a 100 m x 2 m transect, n = 16 transects).                           

The insect pollinator specimens from species observed visiting focal and non-focal C. segetum on the farm were classified into different pollinator functional groups based on species traits likely to play a role in the genetic component of pollination effectiveness (e.g. degree of life-cycle dependence on flowers, mobility, body size, sociality, sex, hairiness, foraging behaviour).                         

33 focal maternal plants were randomly selected from the 144 focal plants for genotyping the maternal plants and their progeny (17 randomly selected offspring per maternal plant, out of which at least 15 were successfully genotyped) at 8 loci (microsatellite markers).

Each experimental unit is a focal C. segetum maternal plant (n = 33).

The related study was based on data from column A to column R. Columns S to AC were not used in the analyses, but are provided in case they would be needed in further analyses.