Parallel evolution of angiosperm colour signals: common evolutionary pressures linked to hymenopteran vision

Abstract

Flowering plants in Australia have been geographically isolated for more than 34 million years. In the Northern Hemisphere, previous work has revealed a close fit between the optimal discrimination capabilities of hymenopteran pollinators and the flower colours that have most frequently evolved. We collected spectral data from 111 Australian native flowers and tested signal appearance considering the colour discrimination capabilities of potentially important pollinators. The highest frequency of flower reflectance curves is consistent with data reported for the Northern Hemisphere. The subsequent mapping of Australian flower reflectances into a bee colour space reveals a very similar distribution of flower colour evolution to the Northern Hemisphere. Thus, flowering plants in Australia are likely to have independently evolved spectral signals that maximize colour discrimination by hymenoptera. Moreover, we found that the degree of variability in flower coloration for particular angiosperm species matched the range of reflectance colours that can only be discriminated by bees that have experienced differential conditioning. This observation suggests a requirement for plasticity in the nervous systems of pollinators to allow generalization of flowers of the same species while overcoming the possible presence of non-rewarding flower mimics.

Figure 1.

Example floral spectral reflections of two Australian native flowers (endemic): Hibbertia scandens (dashed lines, human yellow) and Pandorea jasminoides (solid line, human pink). The arrows show the slope midpoints [25].

Figure 2.

Relative frequency of Australian native plant flowers (n = 111 flowers; highest column n = 19 step functions) having reflectance curve slope midpoints (black bars) compared with the inverse Δλ/λ wavelength discrimination function (solid curve) of the honeybee [24]. The insert shows data for flowers from Israel (n = 180 flowers; highest column n = 36 step functions) from a previous study that used the same methodology [25]. Australia is geologically well separated in space and time from the rest of the world and has a distinctive bee fauna [30]; the data suggest parallel evolution of many angiosperm flower signals to be best discriminated by hymenopteran trichromats.

Figure 3.

Relative frequencies of Australian native plant flower distributions (main figure solid line) compared with a previous study on flower evolution in the Middle East (dashed line, [28]). Data are plotted considering the visual system of hymenoteran trichromats in a hexagon colour space (see insert (i)), and the frequency with which flower colour loci were distributed in 10° sectors (see insert (ii); 0° is at the 12 : 00 angle in the colour hexagon and angles on the abscissa of the main figure read clockwise from 12 : 00) of the colour space. A similar distribution of flower colours has evolved in Australia and the Middle East, despite a very long geological separation of these study sites.

Figure 4.

Colour discrimination (data from Dyer [50]) of stimuli by bumblebees (Bombus terrestris) considering either differential- (dashed line) or absolute- (solid line) conditioning relative to the perceptual distance in a hexagon colour space for hymenopteran colour vision (mean ± s.d.). Horizontal bars show colour distance for which: (i) colours are below threshold for either differential or absolute conditioning, (ii) colours are only reliably discriminated by bees that have experienced differential conditioning, or (iii) colours are reliably discriminated by bees even with only absolute conditioning. The variability in Australian native flowers of the same species (n = 111 flowers; mean ± s.d.) lies within the colour discrimination region where similar colours are only discriminated if bees have received differential conditioning (see text for statistics).