Out on a limb, or a new branch of signalling theory?

Abstract

Could it be that one of nature's most dazzling displays is just a ‘keep out’ sign to insects? According to Hamilton and Brown's recent analysis 1xAutumn tree colours as a handicap signal. Hamilton, W.D. and Brown, S.P. Proc. R. Soc. London B Biol. Sci. 2001; 268: 1489–1493Crossref | Scopus (120)See all References1 of published data, the autumnal change in leaf colour of temperate deciduous trees is a handicap signal to their insect pests, revealing the commitment of the trees to defence. This is the first costly handicap signal to be proposed in plants 2xThe origin of autumn colours by coevolution. Archetti, M. J. Theor. Biol. 2000; 205: 625–630Crossref | PubMed | Scopus (90)See all References2. In animals, handicap signals are often behavioural: stotting in Thompson's gazelles being the most commonly cited example. The scope for handicap signals in plants is perhaps more limited, at least to our current view, but the area of plant–herbivore interactions is one in which they could evolve.Several conditions for a handicap signalling system between deciduous trees and their insect pests appear to be met. First, leaf colour change is costly. Greater percentages of chlorophylls than of carotenoids are resorbed before abscission, and, combined with the early cessation of photosynthesis and the production of other pigments in autumn leaves, it is difficult to view this process as a mere side effect of senescence. Second, the signal must be received. Some aphid species display a sensory bias towards yellow-green light, apparently preferring a dilute hue of the most attractive colour, which might provide a mechanism for host choice based on relative display intensity. Third, the signal should ultimately confer differential reproductive success. Pre-emptive antixenotic signalling, exploiting a pre-existing sensory bias, should protect the tree from both the effects of herbivory and any potentially damaging pathogens that their insect pests might be carrying.For the signal to remain honest, there must be a link between it and the quality (here defensive commitment) being signalled. In this case, there are two ways in which this might be true. Chemical changes in the leaf that result in the autumn colour display could be associated with the production of inhibitors that prevent germination of seedlings through the leaf litter. Aphids could therefore use leaf brightness as a means of assessing the overall energetic investment of the plant in defence. Alternatively, the colour change could be a visual call to arms: systems in which insect-damaged plants produce signals to attract other predatory insects are known 3xExperimental evidence that plants under attack may benefit from parasitoids. Fritzsche-Hoballah, M.E. and Turlings, T.C.J. Evol. Ecol. Res. 2001; 3: 553–565See all References3. Either way, the fact that a tree can produce a vivid display would provide useful information to insects seeking a host.The key, as always, lies in variation. The authors readily point out that only empirical tests will reveal the truth of their hypothesis, and suggest several potential veins of research at both the intra- and interspecific levels. In addition, some of their assumptions must be validated, particularly that specialist pests are more damaging to hosts than are generalist ones, and that the energetically costly autumn display is produced at the expense of some other function. However, this does not detract from a tantalizing idea that will no doubt spark an explosion of new research. Autumn will never be the same again.