B w y o r

Fig. 6.4. The color preferences of seven species of bumble bees (Bombus) superimposed on their phylogeny (Williams 1994). Each bee was experimentally naive at the start of the experiment, and only the first foraging bout was evaluated. Bees were individually tested in a flight arena; they were offered the colors v-violet (bee UV-blue); b-blue (bee blue); w-white (bee blue-green); y-yellow; o-orange; r-red (the latter three are all bee green). Column height denotes the percentage of cumulative choices of all bees from all colonies. Whiskers show percentages for colonies with extreme values.

B. terrestris sassaricus from Sardinia [133; 4; 4518], B. terrestris xanthopus from Corsica [58; 2; 2678], and B. terrestris canariensis from the Canary Islands [159; 5; 3904]. The rationale for testing island populations was that evolution often takes a different course there. Generally, the effects of chance, including those of bottleneck events, will be more manifest on islands than in large mainland populations (Adkison 1995; Barton 1998). In addition, small populations might adapt more readily to local conditions, whereas in large populations, gene flow across long distances may prevent local adaptation (Ford 1955; Stanton & Galen 1997). On the other hand, polymorphism, the raw material for evolution, is lost more easily in small populations, and deleterious mutations may spread through island populations more readily. A dramatic example known from the visual system are the totally color-blind people of Pingelap Island (Hussels & Morton 1972; Chittka & Briscoe 2001). The island populations of B. terres-tris are particularly interesting because they are genetically diferentiated from each other and from the mainland population, whereas the entire mainland population, which stretches all through central, southern, and eastern Europe, appears to be genetically more homogenous (Estoup et al. 1996; Widmer et al. 1998).

Correspondingly, we find no strong differences in color preferences among the mainland B. terrestris populations: all showed the same strong preference for violet-blue shades as the other species above. But some island populations show an additional red preference (Fig. 6.5). In B. t. sas-saricus, this preference is stronger than that for blue colors in some colonies, and is highly significant in all colonies (significance is determined both by a sign test [number of individuals per colony which prefer red over yellow] and a xz 2 x 2 table [colony choices for red vs. yellow]. In all colonies, both tests yielded similar results). In B. t. canariensis, four of five colonies showed a significant preference for red over yellow and orange. The adaptive significance of such red preference is not easy to understand. Some red, UV-absorbing, and pollen-rich flowers exist in the Mediterranean basin, particularly the eastern part, with the highest concentration in Israel (Dafni et al. 1990). In Israel, however, bumble bees do not show red preference, and the red flowers there appear to be predominantly visited by beetles (Dafni et al. 1990). Some of the red species exist in Sardinia, too, but we do not know to what extent they are exploited by bumble bees. The Canary Islands harbor several orange-red flower species (Vogel et al. 1984). These are probably relics of a Tertiary flora, and some seem strongly adapted to bird pollination. In fact, bird visitation has been observed at least in some of these species, but their use by bees is unknown (Vogel et al. 1984; Olesen 1985). Thus, we are left with an interesting observation: flower color preferences are clearly variable within B. terrestris, but we cannot easily correlate the color preferences in different habitats with differences in local flower colors. The possibility that genetic drift has produced the color preferences in some island populations certainly deserves consideration. To explore this possibility further, it will be necessary to sample the local floral market in more detail (as in Menzel & Shmida 1993; Giurfa et al. 1995) and to test whether red preference might simply evolve in some island populations because it is not selected against. We hope to measure the impact on foraging performance and fitness of among-colony variation in preference.

Finally, the observed patterns of floral-color preferences within bumble bees suggest that it may be worthwhile to take a closer look at the receptor level. Could some species of bumble bees (such as B. occidentalis) or some island populations of B. terrestris have actually evolved red receptors.? Clearly, the observation of red preference itself cannot be taken as evidence for the existence of red receptors, because detection and identification of red flowers is possible without specific red receptors (Chittka &

Bombus Franklini Range Map
Fig. 6.5. Biogeography of floral color preferences in Bombus terrestris. Cross-hatched area: distribution of B. terrestris (this range was provided with kind permission by Prof. Pierre Rasmont; the full map will appear in Rasmont etal. 2001). For further explanation, see Fig. 6.4.

Waser 1997). Red flowers do take substantially longer to detect (see above), so that the evolution of red receptors might be favored in species whose ranges overlap with that of red flowers. If physiological research does reveal the existence of red receptors in bumble bees with red preference, we envision two possible evolutionary paths towards such receptors in bees. In large populations, red receptors might become fixed only in the case of a strong selective advantage, such as in bees that already exploit red flowers. Conversely, if the fitness advantage conferred by red receptors is comparatively small, new mutants that carry such receptors might be eliminated by genetic drift with very high probability. In the case of such a minor adaptive advantage, red receptors might spread only through relatively small populations, such as those on islands.

Conclusion

We have used flower colors and bee color vision to convey the message that evolutionary matching of signals and receivers will not happen as readily and easily as physiological adaptation of, say, a receptor's sensitivity. In fact, this work contains a number of cases where behavioral, sensory, and floral traits can be better explained by the species' phyloge-netic history or constraints than by the assumption that each trait in each species is individually and optimally tailored to its environment. Many paths along the way from genes to traits are intertwined, so that evolutionary changes in one trait may render another trait less efficient or nonfunctional. Finally, selection acts on individuals, and whether individuals survive and reproduce depends not only on their genetic quality, and certainly not only on the quality of any trait in which one happens to be interested. Chance plays an important role, and the role it plays will depend on the strength of selection (or the adaptive value of the trait in question) combined with population size and stability. We encourage readers to consider these ideas when studying the evolutionary tuning of flower signals and insect sensory systems, and to design more studies that specifically test for the above possibilities. If we take alternatives to adaptation seriously, we may ultimately understand adaptation better.

Acknowledgements

This study was supported by DFG grants CH 147/1-2 and CH 147/2-1 to L. Chittka. For discussions or help with the experiments we thank S. Armbruster, A. Gerber-Kurz, P. F. Roseler, J. D. Thomson, and N. M. Waser.

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