Geographic Mosaics of Fly Pollinators With Divergent Color Preferences Drive Landscape-Scale Structuring of Flower Color in Daisy Communities.

Allan G Ellis,Bruce Anderson,Jurene E Kemp

doi:10.3389/fpls.2021.617761

Abstract

The striking variation in flower color across and within Angiosperm species is often attributed to divergent selection resulting from geographic mosaics of pollinators with different color preferences. Despite the importance of pollinator mosaics in driving floral divergence, the distributions of pollinators and their color preferences are seldom quantified. The extensive mass-flowering displays of annual daisy species in Namaqualand, South Africa, are characterized by striking color convergence within communities, but also color turnover within species and genera across large geographic scales. We aimed to determine whether shifts between orange and white-flowered daisy communities are driven by the innate color preferences of different pollinators or by soil color, which can potentially affect the detectability of different colored flowers. Different bee-fly pollinators dominated in both community types so that largely non-overlapping pollinator distributions were strongly associated with different flower colors. Visual modeling demonstrated that orange and white-flowered species are distinguishable in fly vision, and choice experiments demonstrated strongly divergent color preferences. We found that the dominant pollinator in orange communities has a strong spontaneous preference for orange flowers, which was not altered by conditioning. Similarly, the dominant pollinator in white communities exhibited an innate preference for white flowers. Although detectability of white flowers varied across soil types, background contrast did not alter color preferences. These findings demonstrate that landscape-level flower color turnover across Namaqua daisy communities is likely shaped by a strong qualitative geographic mosaic of bee-fly pollinators with divergent color preferences. This is an unexpected result given the classically generalist pollination phenotype of daisies. However, because of the dominance of single fly pollinator species within communities, and the virtual absence of bees as pollinators, we suggest that Namaqua daisies function as pollination specialists despite their generalist phenotypes, thus facilitating differentiation of flower color by pollinator shifts across the fly pollinator mosaic.

Highlights

Flower color diversity is a striking feature of the angiosperms, with closely-related plant species, and populations within species, frequently varying geographically in flower color or patterning (e.g., Cooley et al, 2008; Ellis and Johnson, 2009; Newman et al, 2012; Muchhala et al, 2014; Wang et al, 2016)
The broad associations between flower color and different pollinator groups offer indirect evidence that pollinators may have played a crucial role in floral color evolution (Fægri and van der Pijl, 1966; Fenster et al, 2004), while selection studies demonstrate more directly that pollinators can select on flower color (Harder and Johnson, 2009; Sletvold et al, 2016)
We show that there are steep clines in the spatial turnover of flower color in the annual daisy species that dominate spring flowering displays in Namaqualand, and that change in dominant community flower color is underlain by strong gradients in the density of the dominant fly pollinators in the system

Summary

Introduction

Flower color diversity is a striking feature of the angiosperms, with closely-related plant species, and populations within species, frequently varying geographically in flower color or patterning (e.g., Cooley et al, 2008; Ellis and Johnson, 2009; Newman et al, 2012; Muchhala et al, 2014; Wang et al, 2016). Pollinator abundances are usually quantified through observations of visits to the focal flowers, with only a few studies employing independent datasets, such as pollinator distribution records (e.g., Waterman et al, 2011; van der Niet et al, 2014) or trapping surveys (e.g., Phillips et al, 2015), to quantify pollinator gradients It is seldom clear whether geographic associations between floral phenotype and pollinator assemblages are the evolved plant responses to underlying spatial mosaics of pollinator availability, or the result of spatially variable outcomes of competitive interactions of co-occurring flowers for pollination services (Muchhala et al, 2014)

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