Genetic basis and dual adaptive role of floral pigmentation in sunflowers

Variation in floral displays, both between and within species, has been long known to be shaped by the mutualistic interactions that plants establish with their pollinators. However, increasing evidence suggests that abiotic selection pressures influence floral diversity as well. Here, we analyse the genetic and environmental factors that underlie patterns of floral pigmentation in wild sunflowers. While sunflower inflorescences appear invariably yellow to the human eye, they display extreme diversity for patterns of ultraviolet pigmentation, which are visible to most pollinators. We show that this diversity is largely controlled by cis-regulatory variation affecting a single MYB transcription factor, HaMYB111, through accumulation of ultraviolet (UV)-absorbing flavonol glycosides in ligules (the ‘petals’ of sunflower inflorescences). Different patterns of ultraviolet pigments in flowers are strongly correlated with pollinator preferences. Furthermore, variation for floral ultraviolet patterns is associated with environmental variables, especially relative humidity, across populations of wild sunflowers. Ligules with larger ultraviolet patterns, which are found in drier environments, show increased resistance to desiccation, suggesting a role in reducing water loss. The dual role of floral UV patterns in pollinator attraction and abiotic response reveals the complex adaptive balance underlying the evolution of floral traits.

Flower Color as Predictor for Nectar Reward Quantity in an Alpine Flower Community

Entomophilous plants have evolved colorful floral displays to attract flower visitors to achieve pollination. Although many insects possess innate preferences for certain colors, the underlying proximate and ultimate causes for this behavior are still not well understood. It has been hypothesized that the floral rewards, e.g., sugar content, of plants belonging to a particular color category correlate with the preference of the flower visitors. However, this hypothesis has been tested only for a subset of plant communities worldwide. Bumble bees are the most important pollinators in alpine environments and show a strong innate preference for (bee) “UV-blue” and “blue” colors. We surveyed plants visited by bumble bees in the subalpine and alpine zones (>1,400 m a.s.l.) of the Austrian Alps and measured nectar reward and spectral reflectance of the flowers. We found that the majority of the 105 plant samples visited by bumble bees fall into the color categories “blue” and “blue-green” of a bee-specific color space. Our study shows that color category is only a weak indicator for nectar reward quantity; and due to the high reward variance within and between categories, we do not consider floral color as a reliable signal for bumble bees in the surveyed habitat. Nevertheless, since mean floral reward quantity differs between categories, naïve bumble bees may benefit from visiting flowers that fall into the innately preferred color category during their first foraging flights.

Genetic basis and dual adaptive role of floral pigmentation in sunflowers

Variation in floral displays, both between and within species, has been long known to be shaped by the mutualistic interactions that plants establish with their pollinators. However, increasing evidence suggests that abiotic selection pressures influence floral diversity as well. Here we analyze the genetic and environmental factors that underlie patterns of floral pigmentation in wild sunflowers. While sunflower inflorescences appear invariably yellow to the human eye, they display extreme diversity for patterns of ultraviolet pigmentation, which are visible to most pollinators. We show that this diversity is largely controlled by cis-regulatory variation at a single MYB transcription factor, HaMYB111, through accumulation of UV-absorbing flavonol glycosides. As expected, different patterns of ultraviolet pigments in flowers have a strong effect on pollinator preferences. However, variation for floral ultraviolet patterns is also associated with environmental variables, especially relative humidity, across populations of wild sunflowers. Larger ultraviolet patterns, which are found in drier environments, limit transpiration, therefore reducing water loss. The dual role of floral UV patterns in pollination attraction and abiotic responses reveals the complex adaptive balance underlying the evolution of floral traits.

Bumblebees can detect floral humidity

Floral humidity, a region of elevated humidity in the headspace of the flower, occurs in many plant species and may add to their multimodal floral displays. So far, the ability to detect and respond to floral humidity cues has been only established for hawkmoths when they locate and extract nectar while hovering in front of some moth-pollinated flowers. To test whether floral humidity can be used by other more widespread generalist pollinators, we designed artificial flowers that presented biologically-relevant levels of humidity similar to those shown by flowering plants. Bumblebees showed a spontaneous preference for flowers which produced higher floral humidity. Furthermore, learning experiments showed that bumblebees are able to use differences in floral humidity to distinguish between rewarding and nonrewarding flowers. Our results indicate that bumblebees are sensitive to different levels of floral humidity. In this way floral humidity can add to the information provided by flowers and could impact pollinator behaviour more significantly than previously thought.

Selection for two different mating systems in Aquilegia canadensis

Because plants are sessile, they depend on biotic and/or abiotic vectors to transfer pollen from the male pollen-producing anthers to the female pollen-receiving stigmas. As a result, plant mating systems evolve through selection on the floral traits that influence how much pollen is transferred from anthers to stigmas within flowers (self-pollination) vs. between flowers on different individuals (outcrossing). Thus, mating systems are influenced by the traits that dictate the relative abundance of self-versus outcrossed pollen on stigmas. Spatial separation between anthers and stigmas within flowers (herkogamy) is expected to regulate self-pollination yet there are few estimates of how natural selectin acts on this trait. Aquilegia canadensis (columbine, Ranunculaceae) is a short-lived herbaceous plant of rocky outcrops throughout eastern North America that makes seed through both self-fertilization which is influenced by herkogamy, and outcrossing, which is likely influenced by the plant’s floral display size (flower number and size). Selfing provides reproductive assurance in natural populations of columbine, whereas outcrossing appears to produce much fitter offspring, and there is a trade-off between thes two components of the mating system. We, therefore, predicted correlational selection between herkogamy and display size: selection would favour reduced herkogamy among individuals with small floral displays (to enhance reproductive assurance) and increased herkogamy among individuals with large floral displays (to reduce selfing when outcrossing is likely). We tested this prediction by using multivariate linear regression to estimate phenotypic selection through seeds/fruit and seeds/plant on floral traits and plant size for 1015 plants from nine populations of A. canadensis at the Queen’s University Biological Station. Although we detected positive direction selection on display size mostly through flower number, we did not detect selection on herkogamy or correlational selection between herkogamy and display size. As expected, large size is universally favoured yet selection of floral morphology is weak.

Bumblebees can detect floral humidity

Floral humidity, a region of elevated humidity proximal to the flower, occurs in many plant species and may add to their multimodal floral displays. So far, the ability to detect and respond to floral humidity cues has been only established for hawkmoths when they locate and extract nectar while hovering in front of some moth-pollinated flowers. To test whether floral humidity can be used by other more widespread generalist pollinators, we designed artificial flowers that presented biologically-relevant levels of humidity similar to those shown by flowering plants. Bumblebees showed a spontaneous preference for flowers which produced higher floral humidity. Furthermore, learning experiments showed that bumblebees are able to use differences in floral humidity to distinguish between rewarding and nonrewarding flowers. Our results indicate that bumblebees are sensitive to different levels of floral humidity. In this way floral humidity can add to the information provided by flowers and could impact pollinator behaviour more significantly than previously thought.Summary statementWe demonstrate for the first time that bumblebees show a preference to elevated floral humidity and can learn to distinguish flowers that differ in floral humidity levels.

How Are the Flower Structure and Nectar Composition of the Generalistic Orchid Neottia ovata Adapted to a Wide Range of Pollinators?

Plant-pollinator interactions significantly influence reproductive success (RS) and drive the evolution of pollination syndromes. In the context of RS, mainly the role of flower morphology is touched. The importance of nectar properties is less studied, despite its significance in pollination effectiveness. Therefore, the aim of this study was to test selection on flower morphology and nectar chemistry in the generalistic orchid Neottia ovata. In 2019–2020, we measured three floral displays and six flower traits, pollinaria removal (PR), female reproductive success (FRS), and determined the soil properties. The sugars and amino acids (AAs) were analyzed using the HPLC method. Data were analyzed using multiple statistical methods (boxplots, ternary plot, one-way ANOVA, Kruskal-Wallis test, and PCA). Variation of flower structure and nectar chemistry and their weak correlation with RS confirms the generalistic character of N. ovata. In particular populations, different traits were under selection. PR was high and similar in all populations in both years, while FRS was lower and varied among populations. Nectar was dominated by glucose, fructose, and included 28 AAs (Ala and Glu have the highest content). Sugars and AAs influenced mainly FRS. Among soil parameters, carbon and carbon:nitrogen ratio seems to be the most important in shaping flower structure and nectar chemistry.

Noisy communities and signal detection: why do foragers visit rewardless flowers?

Floral communities present complex and shifting resource landscapes for flower-foraging animals. Strong similarities among the floral displays of different plant species, paired with high variability in reward distributions across time and space, can weaken correlations between floral signals and reward status. As a result, it should be difficult for foragers to discriminate between rewarding and rewardless flowers. Building on signal detection theory in behavioural ecology, we use hypothetical probability density functions to examine graphically how plant signals pose challenges to forager decision-making. We argue that foraging costs associated with incorrect acceptance of rewardless flowers and incorrect rejection of rewarding ones interact with community-level reward availability to determine the extent to which rewardless and rewarding species should overlap in flowering time. We discuss the evolutionary consequences of these phenomena from both the forager and the plant perspectives. This article is part of the theme issue ‘Signal detection theory in recognition systems: from evolving models to experimental tests’.