The shared and separate roles of aposematic (warning) coloration and the co-evolution hypothesis in defending autumn leaves

The potential anti-herbivory functions of colorful (red and yellow) autumn leaves received considerable attention in the last decade. The most studied and discussed is the co-evolutionary hypothesis, according to which autumn coloration signals the quality of defense to insects that migrate to the trees in autumn. In addition to classic aposematism (repellency due to signaling unpalatability, non profitability of consumption, or danger for whatever reasons) that operates immediately, this hypothesis also proposes that the reduced fitness of the insects is in their next generation hatching in the spring from eggs laid on the trees in autumn. Supporters of the co-evolutionary hypothesis either posited that this hypothesis differs from visual aposematism or ignored the issue of aposematism. Interestingly, other authors that cited their papers considered the co-evolutionary hypothesis as visual aposematism. Recently, the overlap between the co-evolutionary hypothesis and visual aposematism was finally recognized, with the exception of yellow autumn leaves not signaling defense to aphids, which are known to be attracted to yellow leaves. However, the detailed relationships between these two hypotheses have not been discussed yet. Here I propose that the co-evolutionary hypothesis generally equals visual aposematism in red and yellow autumn leaves towards all herbivores except for yellow not operating with aphids. The co-evolutionary signaling extends beyond classic aposematism because it may operate later and not only immediately. The possibility that for yellow autumn leaves the co-evolutionary hypothesis may also operate via olfactory aposematism should not be dismissed.Key words: aposematic, autumn coloration, co-evolution, defense, evolution, herbivory, treesColorful (red and yellow) autumn leaves dominate large areas of America, Asia and Europe, expressed by thousands of tree, shrub and climber species.^1–5 In the last decade, this phenomenon received considerable scientific attention. For a long time it was a common belief that this coloration is the by-product of the cessation of masking by chlorophylls that degrade in autumn. However, two key theoretical and experimental developments stimulated the recent wave of study of autumn leaf coloration. The first was the recognition that anthocyanins are synthesized de novo in red autumn leaves,^1,2 and the second was the formulation of the anti-herbivory co-evolutionary hypothesis.^6–8The updated version of the co-evolutionary hypothesis⁹ posits that red autumn coloration signals to all types of insects (including aphids) that migrate to the trees in autumn about their chemical defense, lower nutritional quality or imminent leaf fall, or any other characteristic that would induce a lower fitness in the insects. In addition, yellow leaves signals the same to all herbivores except aphids. A special aspect of the co-evolutionary hypothesis is that the reduced fitness of the insects is not only immediate, reducing insect feeding in autumn, but also related to the reduced development of the next generation that hatches in the following spring from eggs laid on the trees in the autumn.⁹ Originally, the co-evolutionary hypothesis addressed both red and yellow autumn leaves.^6–8 However, with the later understanding that yellow leaves usually attract rather than repel aphids,^9–13 the co-evolutionary hypothesis was later restricted to red leaves when aphids are concerned.⁹In addition to other various potential anti-herbivory roles,^14,15 red autumn leaf coloration has several potential physiological functions, such as protection from photoinhibition and photo oxidation, and other physiological functions have been proposed but not agreed upon.^{1,2,9,16–21}