Modularity and evolution of flower shape: the role of function, development, and spandrels in Erica

Abstract

Summary Flowers have been hypothesized to contain either modules of attraction and reproduction, functional modules (pollination‐effecting parts) or developmental modules (organ‐specific). Do pollination specialization and syndromes influence floral modularity? In order to test these hypotheses and answer this question, we focused on the genus Erica: we gathered 3D data from flowers of 19 species with diverse syndromes via computed tomography, and for the first time tested the above‐mentioned hypotheses via 3D geometric morphometrics. To provide an evolutionary framework for our results, we tested the evolutionary mode of floral shape, size and integration under the syndromes regime, and – for the first time – reconstructed the high‐dimensional floral shape of their most recent common ancestor. We demonstrate that the modularity of the 3D shape of generalist flowers depends on development and that of specialists is linked to function: modules of pollen deposition and receipt in bird syndrome, and access‐restriction to the floral reward in long‐proboscid fly syndrome. Only size and shape principal component 1 showed multiple‐optima selection, suggesting that they were co‐opted during evolution to adapt flowers to novel pollinators. Whole floral shape followed an Ornstein–Uhlenbeck (selection‐driven) evolutionary model, and differentiated relatively late. Flower shape modularity thus crucially depends on pollinator specialization and syndrome.

Pollination syndromes in the 21st century: where do we stand and where may we go?

“…The relative position of the corolla and the reproductive organs is decisive in mediating fit with the pollinators and assuring pollen transfer. Recent advances in obtaining detailed 3D‐flower models through high‐resolution X‐ray computed tomography (HRXCT) now provide the necessary basis for studying flower shape variation through landmark‐based geometric morphometrics without losing information on the spatial arrangement of floral organs (van der Niet et al ., 2010; Sedeek et al ., 2014; Wang et al ., 2015; Wilson et al ., 2017; Dellinger et al ., 2019c; Kellenberger et al ., 2019; Reich et al ., 2020). A wide array of methods is available and constantly being expanded, allowing for statistical analyses of multivariate quantitative trait datasets (Table 2).…”

“…Despite this overall (functional) integration, the above‐mentioned processes may influence different parts of the flower differently, potentially leading to different (functional) modules within the flower (Armbruster, 2014; Esteve‐Altava, 2017). Recent macroevolutionary analyses have indeed demonstrated that such functional modules may evolve independently of each other, that is along different trajectories and at different rates, in response to pollinator‐mediated selection (Opedal, 2019; Dellinger et al ., 2019c; Reich et al ., 2020). This relative evolutionary independence of functional modules has been proposed to facilitate (and hence explain the frequent occurrence of) shifts between pollination syndromes in closely related plant species (Armbruster, 2014).…”

“…Second, pollinator shifts could disrupt both type and strength of correlation structures within flowers and change functional modules (Dellinger et al ., 2019c; Reich et al ., 2020). And third, the modularity of specialised flowers was found to be structured by function, while modularity of generalised flowers was structured by developmental affinities of floral organs (Reich et al ., 2020). It will be interesting to relate these results to advertisement traits to understand more deeply their interplay during pollinator shifts and, potentially, speciation.…”

Automatic Identification of First-Order Veins and Corolla Contours in Three-Dimensional Floral Images

“…(2017) examined the association of 3D petal traits and the genotypes in a hybrid line of Sinningia cultivars. Reich et al. (2019) identified the modularity and evolution of 3D flower shapes in Erica species.…”

Paucity of natural history data impedes phylogenetic analyses of pollinator‐driven evolution

“…S1 Floral biology and insect visitation rates of Erica gracilis . Notes S1 Statistical analysis and discussion of floral visitor data for Erica gracilis included in the study of Reich et al (2020). Table S1 Published pollinator data available for Erica spp.…”