Is sexual organ reciprocity related to legitimate pollen deposition in distylous Pulmonaria (Boraginaceae)?

Abstract

Heterostyly, i.e. the reciprocal positioning of anthers and stigmas, is a floral polymorphism that is thought to promote disassortative (i.e. between‐morph) pollination and to maintain genetic diversity within populations. Recent research, however, has shown several cases of heterostylous plant species in which the reciprocal positioning of the sexual organs varies, which may affect the likelihood of ‘legitimate’ pollination between compatible morphs, and hence morph fitness and ultimately the stability of this floral polymorphism. In this study, we investigated floral morphology and stigmatic pollen deposition patterns in nine Pulmonaria species (Boraginaceae) across Europe to test the hypothesis that sexual organ reciprocity is related to legitimate pollen deposition. We used a recently developed adaptive accuracy concept to assess the level of reciprocity and to relate inaccuracies in positioning of sexual organs to legitimate pollen deposition measured on stigmas in the field. The nine investigated Pulmonaria species showed substantial deviations from perfect reciprocity, with total inaccuracies varying between 2.9 and 20.3% relative to the squared mean of all anther and stigma heights in the population. In almost all cases, most of the inaccuracy was generated by the high‐level organs. Total pollen deposition was always higher on stigmas of long‐styled individuals, but stigmas of short‐styled individuals received significantly more legitimate pollen than stigmas of long‐styled individuals (71.23% and 38.75% respectively). We also found a weak but significant relationship between measures of inaccuracy and the level of disassortative pollination. Under these conditions of pollen flow, the distylous mating system is predicted to persist in only eleven (27%) of all sampled populations. Overall, these results indicate that deviations from perfect reciprocal herkogamy are common in Pulmonaria and have an impact on legitimate pollen deposition.

The impact of individual inaccuracy of reciprocal herkogamy on legitimate pollen deposition and seed set in a distylous self‐incompatible herb

“…In the distylous genus Pulmonaria , Jacquemyn et al () recently calculated inaccuracy values for a large number of populations over nine species across Europe, and documented mean 2 ‐standardized total inaccuracy values that usually varied between 4 and 11. Only in the case of an Estonian population of Pulmonaria obscura , an inaccuracy value >20 was observed.…”

“…However, in a third species ( P. veris ), a strikingly different pattern was observed with total inaccuracy and imprecision being affected by high and low organs to similar extents (Armbruster et al, ). Detailed assessment of pollen deposition patterns on stigmas of Pulmonaria further showed that the percentage of legitimate pollen deposition significantly decreased with increasing individual inaccuracy, suggesting that deviations from perfect reciprocal herkogamy may be much more common in heterostylous plant species than previously assumed and have a significant impact on pollen transfer patterns (Jacquemyn et al, ).…”

“…Apart from insect‐specific differences in pollen uptake, flowers of heterostylous plant species have also been found to show deviations from perfect reciprocity (Armbruster et al, ; Eckert & Barrett, ), potentially further affecting pollen deposition patterns. Recent observations in nine Pulmonaria species have shown that most species showed deviations from perfect reciprocity, with total inaccuracies varying between 2.9% and 20.3% relative to the squared mean of all anther and stigma heights in the population (Jacquemyn, Gielen, & Brys, ). In almost all cases, most of the inaccuracy was generated by the high‐level organs.…”

Climate change increases ecogeographical isolation between closely related plants

“…Members of Pulmonaria tend to lack prezygotic barriers to mating as they have strong overlapping distributions, share pollinators (mostly bumblebees and other bees), and many produce hybrids (Meeus, Jansens, Helsen, & Jacquemyn, ; Sauer, ). Consequently, species delimitation within Pulmonaria has proven to be problematic (Bolliger, ; Meeus et al., ), as these species are morphologically similar with all having pinkish‐blue, actinomorphic, tube‐shaped flowers (Jacquemyn, Gielen, & Brys, ) and hairy leaves. In fact, Darwin () considered many Pulmonaria taxa as varieties of the same species.…”

Inacurácia em espécies distílicas de Rubiaceae

“…In distylous plants, the reciprocal position of anthers and stigmas is the main characteristics that promote the disassortative pollination among morphs and limit selfing and sexual interference Keller et al 2014;Jacquemyn et al 2015). Variations in the inaccuracies of organs cause deviations in the level of reciprocal position and can lead to ineffective pollen flow and pollen limitation, which can affect the reproductive production in one or both morphs types (Faivre and McDade, 2001;Jacquemyn et al 2015;Jacquemyn et al 2018). Since all the populations studied are typically distylous, any change of the reproductive organs positions would result in collapse and a possible breakdown in the system.…”