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

Abstract

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.

Colorful (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.^6–8

The 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.⁹

In 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}

Visual Aposematism

Aposematic (warning) coloration is a biological phenomenon in which poisonous, dangerous or otherwise unpalatable organisms visually advertise these qualities to animals. The evolution of aposematic coloration is based on the ability of target enemies to associate the visual signal with the risk, damage or non-profitable handling, and later to avoid such organisms as prey. Typical colors of aposematic animals are yellow, orange, red, purple, black, white and brown and combinations of these,^22–25 and the same is true of visually aposematic plants.^26,27

Many types of aposematic coloration may simultaneously serve physiological, communicative and other defensive functions as well.^9,15,25,27 Therefore, since it is difficult in many cases to evaluate the relative share of the various physiological and defensive roles of autumn leaf coloration and identify the specific selective agents involved in their evolution, the relative contribution of these roles in the evolution of autumn leaf coloration is not well understood yet.

Contrasting views on the phenomenon of bright autumn leaf coloration have been presented concerning the hypothesis that these leaves may be aposematic. Archetti,⁶ in the first paper presenting the co-evolutionary hypothesis, specifically rejected the possibility that these leaves are visually aposematic in his discussion of the defensive signaling by red and yellow autumn leaves to aphids. The major general theoretical progress of the co-evolutionary hypothesis was the demonstration of a potentially broad operation of Zahavi's handicap principle in plants. It is important to view this definition in the light of the theoretical understanding of the time, since aposematism was not considered to be a handicap at the time.²⁸ In other studies that favored the co-evolutionary signaling hypothesis,^7,8,29–31 aposematism was not discussed. Interestingly, Lee and Gould,¹⁷ Lee,³² Gould,¹⁹ Sherratt et al.³³ Karageorgou and Manetas,³⁴ Manetas,³⁵ Chittka and Döring,¹² Schaefer and Rolshausen³⁶ and Karageorgou et al.³⁷ interpreted the co-evolutionary hypothesis of autumn coloration presented in the papers by Archetti,⁶ Hamilton and Brown⁷ and Archetti and Brown⁸ as a case of visual aposematism (warning coloration), in spite of the authors' differing view.

When the red-colored autumn leaves are well defended by various chemicals because of shared biosynthetic pathways, as proposed by Schaefer and Rolshausen,³⁸ or when yellow autumn leaves are poisonous, they should be considered aposematic.^{9,15,21,27,39,40} Recently, Archetti⁴⁰ and Archetti et al.⁹ accepted that there is an overlap between the co-evolutionary and visual aposematic hypotheses, but the fine details and degree of overlap of the two hypotheses have only been partly elaborated yet,⁴⁰ and a more detailed view is the purpose of this discussion.

Olfactory Aposematism

Visual aposematism of red and yellow autumn leaves may not be the only type of aposematism expressed by autumn leaves. Olfactory aposematism, whereby poisonous plants deter mammalian or insect herbivores, has been proposed to operate in plants.^41–45 Holopainen⁴⁶ presented data strongly indicating the involvement of olfactory aposematism in autumn leaves. In addition, the fact that there are good physiological measurements of significant volatile release from autumn leaves⁴⁷ supports the possibility of the operation of olfactory aposematism by these leaves simultaneously with visual aposematism.

Conclusions

I propose that the relationships between the co-evolutionary and aposematic hypotheses are as follows: the co-evolutionary hypothesis concerning red and yellow autumn leaves indeed equals aposematism for various herbivorous species for which it is effective, excluding the combination of yellow leaves and aphids. Furthermore, the co-evolutionary hypothesis is actually a mixture of two types of aposematism: (1) delayed aposematism because the purpose of the signaling is to deter egg laying in autumn, and the damaged insects are mainly the ones that would hatch in the following spring, and (2) operates immediately, like classic aposematism. Classic aposematism is aimed towards animals that feed at the time of signaling. The indications for volatile signaling^46,47 raise the possibility that for certain yellow autumn leaves the co-evolutionary hypothesis may operate even towards aphids via olfactory aposematism.

A careful examination of both plant and insect species in each studied case is needed in order to make a precise classification of the signaling: simple immediate aposematism/coevolutionary or only delayed co-evolutionary relationships. The potential role of olfactory aposematism in red, yellow, brown and green autumn leaves has received very little attention,⁴⁶ and deserves much more.

The posited co-evolutionary hypothesis^6–8 was very fruitful in stimulating theoretical discussions and empirical studies on the defense mechanisms of red and yellow autumn leaves. The possibility that classic aposematism, in signaling systems other than red and yellow autumn leaves, has a delayed action has not been considered in depth in general and in plants in particular and needs further study. Studying this aspect of aposematism may be an additional important contribution of the co-evolutionary hypothesis.