The mechanics of pollinator attraction: development and function of floral diffraction gratings

Pattern formation is key to the development of all multicellular organisms. Although biologists traditionally focus on actively controlled patterning systems, many biological patterns are emergent phenomena arising from physical forces acting on materials with specific chemistries. This is an inevitable consequence of the nature of living organisms. While genetic programmes and developmental pathways appear to have great power to sculpt form, they can only do so with materials defined by their chemical properties and in the context of a world dominated by physical forces. All living material is composed of molecules which, according to their types, frequency and organization, will confer particular material properties on the tissue. And all living organisms are subject to physical forces throughout their growth and development. From this perspective, it is not surprising that classical developmental biology cannot account for all patterns. Mechanically-emergent pattern formation has received relatively little attention, until recently, but is now being explored at a variety of system, organ and tissue levels.

One example of a mechanically-emergent pattern is that of epidermal wrinkles, found in both plants and animals. Regular arrays of wrinkles can influence the optical properties of a tissue. For example, elongated rows of wrinkles on the petals of Hibiscus trionum act as a diffraction grating, giving rise to structural colour which can help bumblebees to find targets more quickly. We know very little about how wrinkle patterns, such as the H. trionum petal diffraction grating, form during development, in any tissue in either plants or animals.

Floral diffraction gratings occur infrequently, but have evolved multiple times, suggesting that they are important in pollinator attraction. Bumblebees, used as model pollinators in behavioural studies, find artificial flowers with replica petal diffraction gratings more quickly than controls without them. However, there is considerable debate in the scientific community about whether these experiments with artificial surfaces really replicate natural conditions, and therefore whether floral diffraction gratings really have any impact either on pollinator attraction or on plant fitness.

In this project we will address both the development of the Hibiscus trionum diffraction grating and its function. We have developed a mechanical model which explains the development of the grating through physical forces acting on the tissue, and we have developed the tools to test this model using transgenic approaches to change the plant's tissue properties. As we do this testing, we will produce transgenic plants which lack the diffraction grating, or have altered forms of it. We will use these in behavioural experiments in the lab and in glasshouses to understand fully how the diffraction grating affects pollinator behaviour.

Our project will help scientists to understand how flower forms develop, and also how they function in pollinator attraction.

In this proposal I aim to understand the development of petal diffraction gratings, and their function. Diffraction gratings are regular arrays of surface ridges which interfere with light, generating structural colour. My group has previously described them on the petals of a number of plant species, and shown that artificial replicas of them improve pollinator foraging efficiency and search image formation.

In the first workpackage I aim to understand the development of the diffraction grating. We have already demonstrated that mechanical forces are sufficient to explain the buckling of the Hibiscus petal cuticle (Airoldi et al 2021 Cell Reports), and have tested and disproved a simple model of surface buckling (Moyroud et all 2022 Current Biology). Working with project partner Al Crosby we have developed a detailed bilayer model which we believe may explain the development of the Hibiscus diffraction grating (Lugo-Velez et al, 2022, bioRxiv). In this workpackage we will test that model by transgenic manipulation of the material properties of the developing Hibiscus petal (cuticle stiffness, cell wall stiffness, cuticle thickness) and the forces acting on it (cell curvature, cell anisotropy).

In the second workpackage I aim to define the adaptive role of diffraction gratings. We have previously shown that artificial replicas improve pollinator foraging efficiency, but this has attracted controversy in the literature with some authors arguing that real floral diffraction gratings will not influence pollinators in a natural foraging situation. The transgenic lines produced in workpackage 1 will include flowers with no diffraction grating and flowers with altered diffraction gratings. We will use these both in our bumblebee behavioural lab, and in glasshouse conditions, to explore pollinator responses and, ultimately, the effects on plant fitness.