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

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.

Keywords: Asteraceae (compositae); Diptera; South Africa; flower color; geographic mosaics of pollinators; greater cape floristic region; pollinator driven divergence; sensory drive.

Figure 1

The annual daisy species and their pollinators that characterize orange (A) and white (B) dominated communities in Namaqualand. Dimorphotheca sinuata (C) and Dimorphotheca pluvialis (D) are widespread and dominant in the Kamiesberg and Sandveld bioregions, respectively. Ursinia cakilefolia (E) and Ursinia speciosa (F) are more localized but dominate communities they occur in. The bombyliid flies, Megapalpus capensis (G) and Corsomyza nigripes (H) are dominant pollinators in the orange and white communities, respectively. The inflorescence diameter of the two Dimorphotheca species is on average 35mm, and the diameter of the two Ursinia species is on average 31mm. Both fly species show variation in size but are always smaller than 10mm. Photos: JEK.

Figure 2

Strongly aligned spatial gradients of flower color and pollinators of annual daisy species across the Namaqualand landscape. The non-overlapping distribution (A) and density relationships (B) of the focal orange (Dimorphotheca sinuata, Ursinia cakelifolia) and white (Dimorphotheca pluvialis, Ursinia speciosa) flowered species at 54 sites. The geographic mosaic (C) and density relationships (D) of the dominant bee-fly pollinators, Megapalpus capensis, and Corsomyza nigripes, across 103 survey sites.

Figure 3

The association between dominant flower color and pollinator species densities. Megapalpus capensis (A) and Corsomyza nigripes (B) densities predict flower color of Dimorphotheca and Ursinia species across 54 sites, where Megapalpus capensis is associated with orange flower dominance and Corsomyza nigripes is associated with white flower dominance.

Figure 4

Distinguishability and detectability of daisy flower color in fly vision. Orange flowers are indicated in orange and white flowers in gray throughout. (A) Reflectance spectra of ray florets of the four focal daisy species. Dotted lines indicate Dimorphotheca species, and solid lines show Ursinia species. (B) Flower colors modeled in the Troje (1993) fly color space using Eristalis receptor sensitivities with adaptation against the alternate soil backgrounds. The orange and gray circles indicate orange and white-flowered species, respectively. (C) Difference in detectability, quantified as Euclidean distances from the origin of fly color space, of the orange (Dimorphotheca sinuata, Ursinia cakilefolia) and white (Dimorphotheca pluvialis, Ursinia speciosa) species on the two soil backgrounds (pale and red soils). Species did not contrast significantly more strongly against their native soils (pale for orange flowers, red for white flowers) than foreign soils.

Figure 5

The probability of pollinating flies (Corsomyza nigripes and Megapalpus capensis) choosing an orange flower over a white flower. Experiments tested fly color preferences using orange-white species pairs of Dimorphotheca (orange Dimorphotheca sinuata vs. white Dimorphotheca pluvialis) and Ursinia (orange Ursinia cakilefolia vs. white Ursinia speciosa) presented on both red and pale soils. Megapalpus capensis preferred orange flowers and Corsomyza nigripes preferred white flowers of both daisy genera, irrespective of the background-color.

Figure 6

Detectability of flower color on different background soils as quantified by initial choices of fly pollinators for flowers presented on different soil backgrounds. Corsomyza nigripes (usually found in white floral communities on red soils) chose white flowers (Dimorphotheca pluvialis) on a red soil background significantly more frequently that on pale soil, while Megapalpus capensis (usually found in orange floral communities on pale soils) visited orange flowers (Dimorphotheca sinuata) on both backgrounds with equal frequency. The dashed line indicates the expected choice ratio if there is no difference in detectability across backgrounds.

Figure 7

The effect of color conditioning on the flower color choices of two dominant fly pollinator species. Choice experiments were used to characterize flower color choices before and after conditioning. In the first experiment Corsomyza nigripes and Megapalpus capensis flies were conditioned on flowers of their non-preferred color for 1h, and in a second experiment, Megapalpus capensis flies were forced to feed on non-preferred white flowers for a day. Flower color preferences were not altered by conditioning.