Coevolution and the adaptive value of autumn tree colours: colour preference and growth rates of a southern beech aphid

The evolutionary explanation for the change in leaf colour during autumn is still debated. Autumn colours could be a signal of defensive commitment towards insects (coevolution) or an adaptation against physical damage because of light at low temperatures (photoprotection). These two hypotheses have different predictions: (1) under the coevolution hypothesis, insects should not prefer red leaves in autumn and grow better in spring on trees with green autumn leaves; and (2) under the photoprotection hypothesis, insects should prefer and grow better on trees with red leaves because they provide better nutrition. Studying colour preference in autumn and growth rates in spring of a southern beech aphid species (Neuquenaphis staryi) on Nothofagus alessandrii, we found preference for green leaves in autumn but no differential performance of aphids in spring. We suggest that aphid preference for green might have evolved to exploit better their host during the autumn rather than to improve their performance in spring.     

Evidence from the domestication of apple for the maintenance of autumn colours by coevolution

The adaptive value of autumn colours is still a puzzle for evolutionary biology. It has been suggested that autumn colours are a warning signal to insects that use the trees as a host. I show that aphids (Dysaphis plantaginea) avoid apple trees (Malus pumila) with red leaves in autumn and that their fitness in spring is lower on these trees, which suggests that red leaves are an honest signal of the quality of the tree as a host. Autumn colours are common in wild populations but not among cultivated apple varieties, which are no longer under natural selection against insects. I show that autumn colours remain only in the varieties that are very susceptible to the effects of a common insect-borne disease, fire blight, and therefore are more in need of avoiding insects. Moreover, varieties with red leaves have smaller fruits, which shows that they have been under less effective artificial selection. This suggests a possible trade off between fruit size, leaf colour and resistance to parasites. These results are consistent with the hypothesis that autumn colours are a warning signal to insects, but not with other hypotheses.     

Catching a red herring: autumn colours and aphids

The purpose of this note is not to support any particular hypothesis explaining the evolution of red coloured autumn leaves, but to present evidence that shows existing knowledge does not support one such hypothesis – that red coloured leaves evolved as a signal to protect trees from aphids feeding and laying eggs on them in autumn. An alternative hypothesis is that autumn-feeding aphids are senescence-feeders, evolved to feed only on senescing leaves. These aphids are programmed to detect and feed on such leaves when they are still green and yellow and actively exporting their nutrients. Aphids reject or ignore red leaves because they are no longer good food, not because they are protecting the trees from the aphids.     

Das Geheimnis des roten Herbstlaubes

The secret of the fall colour red The autumnal coloration of trees and shrubs in temperate climate regions is a well‐known spectacle of nature. Crucial for the yellow colour of leaves is the degradation of chlorophylls which cover the yellow colour of carotenoids. Chlorophyll degradation is a prerequisite for protein degradation and remobilization of precious nitrogen in the amino acids of the chloroplast proteins. In some species leaves turn red in autumn by accumulation of anthocyanins. Anthocyanins can reduce photo‐oxidative stress by acting as a sunscreen shielding against the harmful effects of excess light. Furthermore, anthocyanins prevent the landing of insects – in particular aphides.     

Spring versus autumn leaf colours: Evidence for different selective agents and evolution in various species and floras

Red colouration is common in young and old leaves of broadleaf woody species. Assuming that leaf colours are adaptive, we examined, by comparing the colouration in young versus old leaves, the possibility that different selection agents may have operated on spring versus autumn leaf colouration. We observed spring versus autumn colouration in three very different woody floras (Finland, Japan and Israel) in order to allow for a broad ecological and evolutionary spectrum. The null hypothesis was that if the same selective agents operated in spring and autumn, it is expected that when spring leaves are red, they should always be red in autumn, and when spring leaves are green, they should be green or yellow in autumn. We found that green spring leaves are almost exclusively associated with yellow leaf colour at senescence in autumn. Species with red autumn leaves almost always have at least some red colouration in their spring leaves. However, about half of the species with red spring leaves have yellow autumn leaves. Brown autumn leaves were not common in the species we studied. As about half of the species with red spring leaves have yellow autumn leaves but not vice versa, we conclude that there are many cases in which the selecting agents for spring versus autumn leaf colour were not the same.     

Life-history strategies affect aphid preference for yellowing leaves

According to the nutrient-translocation hypothesis, yellowing tree leaves are colonized by aphids at the end of the growing season owing to improved availability of nutrients in the phloem sap after chlorophyll degradation. We measured aphid densities on potted Betula pendula seedlings in a field site where a small proportion of foliage rapidly turned yellow before normal autumn coloration as a consequence of root anoxia. The number of adults and nymphs of the birch-feeding specialist aphids Euceraphis betulae, Betulaphis brevipilosa and Callipterinella tuberculata were counted from leaves on each of the 222 plants. Aphids were detected on 19 per cent of green leaves and on 41 per cent of yellow leaves. There was no indication of aphid avoidance of yellow leaves, and the number of winged (alate) viviparous E. betulae adults and their nymphs were significantly higher on yellow leaves than on green leaves, while the numbers of apterous B. brevipilosa and C. tuberculata did not differ between the leaf colour types. Our result suggests that only aphid species with alate generation during colour change can take advantage of yellowing leaves. This may explain the exceptional abundance of E. betulae compared with other aphid species on birches.     

Aphids do not attend to leaf colour as visual signal, but to the handicap of reproductive investment

The evolution of visual warning signals is well known in animals but has received scant attention in plants. The coevolutionary hypothesis is the most influential hypothesis on warning signals in plants proposing that red and yellow leaf colours in autumn signal defensive strength to herbivores. So far, evidence in support of the hypothesis, which assumes a coevolutionary origin of autumnal leaf colours, is correlative and open to alternative explanations. We therefore tested the coevolutionary hypothesis experimentally by colouring the leaves either red or green of same-aged mountain ash (Sorbus aucuparia) individuals. We monitored the response of winged aphids to leaf colour using insect glue on branches with natural and artificial leaf colours in each individual. In contrast to the prediction of the coevolutionary hypothesis, aphid numbers did not differ between the individuals with artificial green or artificial red leaves. Likewise, at the within-plant level, aphids did not colonize branches with natural green leaves preferentially. However, we suggest that plants emitted warning signals because aphids colonized the hosts non-randomly. We found a strong positive correlation between aphid numbers and fruit production, suggesting an allocation trade-off between investment in plant defence and reproduction. Our study demonstrates that aphids use warning signals or cues in host selection, probably volatiles, but that they did not use leaf colour.     

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}     

What do red and yellow autumn leaves signal?

The widespread phenomenon of red and yellow autumn leaves has recently attracted considerable scientific attention. The fact that this phenomenon is so prominent in the cooler, temperate regions and less common in warmer climates is a good indication of a climate-specific effect. In addition to the putative multifarious physiological benefits, such as protection from photoinhibition and photo-oxidation, several plant/animal interaction functions for such coloration have been proposed. These include (1) that the bright leaf colors may signal frugivores about ripe fruits (fruit flags) to enhance seed dispersal; (2) that they signal aphids that the trees are well defended (a case of Zahavi’s handicap principle operating in plants); (3) that the coloration undermines herbivore insect camouflage; (4) that they function according to the “defense indication hypothesis,” which states that red leaves are chemically defended because anthocyanins correlate with various defensive compounds; or (5) that because sexual reproduction advances the onset of leaf senescence, the pigments might indicate to sucking herbivores that the leaves have low amounts of resources. Although the authors of hypotheses 3, 4, and 5 did not say that bright autumn leaves are aposematic, since such leaves are chemically defended, unpalatable, or both, we suggest that they are indeed aposematic. We propose that in addition to the above-mentioned hypotheses, autumn colors signal to herbivorous insects about another defensive plant property: the reliable, honest, and critical information that the leaves are about to be shed and may thus cause their mortality. We emphasize that all types of defensive and physiological functions of autumn leaves may operate simultaneously.     

Classification of hypotheses on the evolution of autumn colours

I review the hypotheses that have been proposed to explain the adaptive value of autumn leaf colours. The available adaptive hypotheses can be reduced to the following. Photoprotection: pigments protect against photoinhibition or photooxidation allowing a more efficient recovery of nutrients. Drought resistance: pigments decrease osmotic potential allowing leaves to tolerate water stress. Leaf warming: pigments convert light into heat and warm leaves. Fruit flag: colour attracts animals that help disperse seeds. Coevolution: colour signals that the tree is not a suitable host for insects. Camouflage: colour makes leaves less detectable to herbivores. Anticamouflage: colour enhances conspicuousness of parasites dwelling on leaves to predators or parasitoids. Unpalatability: pigments act as direct anti-feedants against herbivores. Reduced nutrient loss: yellow leaves have less to lose against herbivory. Tritrophic mutualism: colour attracts aphids which attract ants that defend the trees from other insects. For each hypothesis I mention the original references, I define assumptions and predictions, and I discuss briefly conceptual problems and available evidence.     

Sexual reproduction advances autumn leaf colours in mountain birch (Betula pubescens ssp. czerepanovii)

Autumnal change in leaf colour of deciduous trees is one of the most fascinating displays in nature. Current theories suggest that autumn leaf colours are adaptations to environmental stress. Here I report that the number of ripening female catkins altered timing of yellow autumn leaf colours in mountain birch. The tree's autumnal colour change was brought forward if the tree matured plenty of female catkins. Since yellow colour pigments in leaves are unmasked as leaf nitrogen is re-translocated, sexual reproduction may alter resource allocation at times of leaf senescence. Thus, our current view on the reasons for leaf senescence has to be re-examined, and a novel evolutionary explanation is needed for the appearance of yellow autumn leaf colours.     

Do aphids paint the tree red (or yellow)—can herbivore resistance or photoprotection explain colourful leaves in autumn?

We explored two mutually nonexclusive hypotheses on autumnal leaf colouration. The co-evolutionary hypothesis states that autumnal leaf colouration functions as a handicap signal to herbivorous insects, whereas the photoprotection hypothesis posits that plant pigments primarily protect the plant against cold-induced photoinhibition and enhance nutrient transfer. To contrast both hypotheses, we compared yellow and red leaf colouration in three groups of mountain ash (Sorbus aucuparia L.). Two montane groups of different age were characterised by low aphid numbers and low temperature, and a lowland group by high aphid numbers and high temperature. There were no consistent altitudinal differences in leaf colouration. Compared to young trees, adult trees developed fewer red but more yellow leaves at high altitude. In the lowland population, the development of red leaf colour was related to decreasing daytime temperature, whereas the appearance of yellow leaf colouration corresponded to the decreasing photoperiod. This is consistent with the photoprotection hypothesis. Individual differences in red and yellow leaf colouration were inversely correlated to the number of fruits, which might be interpreted as a trade-off between reproductive and protective commitment. Temperature effects explained variation in aphid numbers over time and leaf colouration explained aphid distribution on a given day. As predicted by the co-evolutionary hypothesis, strongly coloured individuals harboured fewer aphids than green or dull-coloured ones. Since decreasing temperature reduced the number of migrating aphids but induced red leaf colouration, these processes are not mutually fine-tuned, which likely restricts the potential for co-evolution between mountain ash and aphids.     

不同叶色三叶海棠叶片成色色素分析

结合民族植物学和药理学的研究方法,对西双版纳地区傣族、哈尼族和基诺族等3个少数民族民间利用番石榴（Psidium guajava）、余甘子（Phyllanthus emblica）和水柳（Homonoia riparia）的传统知识进行调查研究及体外抗菌活性实验。结果表明：番石榴和余甘子在村寨中较为常见,当地少数民族将其种植于庭院中,常作为果蔬食用,食用番石榴嫩叶可缓解拉肚子的症状,治疗腹痛、腹泻。水柳生长在水边,傣族会将其叶作为腌酸鱼的配料之一。根据文献记载,番石榴、余甘子和水柳的叶部位作为药使用时,常煎水外洗,治疗皮肤瘙痒。对这3种药用植物叶部位采用80%乙醇浸泡制备的提取物进行体外抗菌实验,结果显示番石榴、余甘子和水柳3种药用植物对金黄色葡萄球菌和大肠埃希菌均有较好的抑菌和杀菌活性,其最小抑菌浓度MIC在98~390 μg·mL 1之间,最小杀菌浓度MBC在98~781 μg·mL 1之间。番石榴和水柳叶对铜绿假单胞菌有一定抑菌和杀菌活性,其MIC和MBC范围均为6 250~12 500 μg·mL 1。由此可见,这3种药用植物的民间利用具有一定的合理性和药用开发价值。     

Loss of autumn colors under domestication: A byproduct of selection for fruit flavor?

According to the coevolution hypothesis the red autumn leaves of certain tree species are a warning signal towards insects that lay their eggs on the trees. A recent study has shown that red leaves are common in wild varieties of apple (Malus pumila) but not in cultivated varieties. This suggests that autumn colors have been lost during domestication due to relaxed selection against insects. The few varieties with red leaves have small fruits, similar to their wild ancestors, which shows that they have been under less effective artificial selection. As expected by the coevolution hypothesis these red varieties are very susceptible to an insect-borne disease, fire blight. Here I report further data on the loss of autumn colors under domestication. Since red leaf color is correlated with red fruit flesh color, if red fruit flesh has more astringent taste it is possible that loss of autumn colors is not only due to relaxed selection against insect, but also to direct artificial selection against astringent taste. However even varieties with yellow flesh turn out to have astringent taste. Moreover, while red fruit flesh is common in cultivated varieties with red leaves, it is very rare in wild varieties. It is unclear, therefore, whether loss of autumn color under domestication was a byproduct of artificial selection against red fruit flesh.Key words: coevolution, autumn colors, signaling, apple, Malus pumila, domestication, artificial selection, germplasm     

Bright autumn colours of deciduous trees attract aphids: nutrient retranslocation hypothesis

We propose an alternative hypothesis to the handicap-signalling hypothesis, to explain the high number of specialist aphids on tree species having bright autumn colour. Since birch aphids actively seek the first yellowing leaves for breeding in autumn, it is obvious that autumn colour of foliage does not repel migrating aphids. We suggest that aphids use bright colours as a cue to detect individual trees and leaves that are good sources of nitrogen in the form of amino acids in autumn. The active formation of bright-coloured pigments in leaves is needed to protect them from photo inhibition during energy consuming nutrient retranslocation under cold autumn conditions. During nutrient export from leaves, nitrogen is in the form of amino acids in the sieve elements and easily available for aphids. Therefore, bright colours may act as a signal of easily available high-quality food for viviparous aphid migrants that are selecting suitable trees for their sexual offspring reproduction. The females of sexual generation grown on the better quality food probably can oviposit the over-wintering eggs to the twigs in higher numbers, which may have an adaptive advantage in competition with conspecific females.     

The origin of autumn colours by coevolution

We lack an adaptive explanation for a striking phenomenon, that of bright colours displayed in autumn by the leaves of many deciduous trees. The usual explanation is that it is simply a non-adaptive secondary effect of leaf senescence. A game-theoretic model of biological signalling provides an adaptive hypothesis for autumn colours showing that they can be the result of a process of coevolution between insects and trees: if leaf colour acts as a warning indicator of the tree's vigour to autumn parasite insects, trees can gain advantage from the reduction of parasite load and insects can gain advantage from location of the most profitable hosts to lay their eggs. The results of the model are consistent with Zahavi's handicap principle. Possible explanations for the origin of the system and evidence from natural history are discussed.     

Autumn tree colours as a handicap signal.

Many species of deciduous trees display striking colour changes in autumn. Here, we present a functional hypothesis: bright autumn coloration serves as an honest signal of defensive commitment against autumn colonizing insect pests. According to this hypothesis, individuals within a signalling species show variation in the expression of autumn coloration, with defensively committed trees producing a more intense display. Insects are expected to be averse to the brightest tree individuals and, hence, preferentially colonize the least defensive hosts. We predicted that tree species suffering greater insect damage would, on average, invest more in autumn-colour signalling than less troubled species. Here, we show that autumn coloration is stronger in species facing a high diversity of damaging specialist aphids. Aphids are likely to be an important group of signal receivers because they are choosy, damaging and use colour cues in host selection. In the light of further aspects of insect and tree biology, these results support the notion that bright autumn colours are expensive handicap signals revealing the defensive commitment of individual trees to autumn colonizing insect pests.     

Association of red coloration with senescence of sugar maple leaves in autumn

We evaluated the association of red coloration with senescence in sugar maple (Acer saccharum Marsh.) leaves by assessing differences in leaf retention strength and the progression of the abscission layer through the vascular bundle of green, yellow, and red leaves of 14 mature open-grown trees in October 2002. Computer image analysis confirmed visual categorization of leaves as predominantly green, yellow or red, and chemical quantification of leaf pigment concentrations verified that leaf color reflected underlying differences in leaf biochemistry. Significantly lower chlorophyll concentrations within red and yellow leaves indicated that senescence was more advanced in leaves from these color categories relative to green leaves. Among leaf types, only red leaves contained high concentrations of anthocyanins. There were significant differences in leaf retention capacity among color categories, with the petioles of green leaves being the most firmly attached to twigs, followed by red and then yellow leaves. Microscopic analysis indicated that yellow leaves had the most advanced extension of the abscission layer through the vasculature, with green and red leaves having significantly less abscission layer progression than yellow. A more limited progression of the abscission layer through vascular bundles may be evidence of delayed leaf senescence that could extend resorption of mobile leaf constituents. Together, results from this study suggest an association between leaf anthocyanin content and functional delays in senescence.     

Importance of olfactory and visual signals of autumn leaves in the coevolution of aphids and trees

Deciduous trees remobilize the nitrogen in senescing leaves during the process of autumn colouration, which in many species is associated with increased concentrations of anthocyanins. Archetti and Hamilton and Brown observed that autumn colouration is stronger in tree species facing a high diversity of specialist aphids. They proposed a coevolution theory that the bright colours in autumn might provide an honest signal of defence commitment, thus deterring migrant aphids from settling on the leaves. So far, there have been very few experimental results to support the hypothesis, and tree commitment to phenolics-based defences has not shown direct protection against aphids. Predators and parasitoids have been found to be the major controllers of arboreal aphids. Indirect defences involve the emission of attractive volatile compounds that enhance the effectiveness of carnivorous enemies. The indirect defence hypothesis is presented to explain low aphid diversity on tree species that are green during autumn. The hypothesis suggests that green foliage can continue to produce herbivore-inducible plant volatiles and maintain volatile-based indirect plant defences against aphids until leaf abscission.     

Flowers for bees,autumn colours for whom? An experimental test with autumn colouration in mountain birches (Betula pubescens ssp. czerepanovii) as a signal against the moth Epirrita autumnata

In 2001, Hamilton and Brown proposed a controversial hypothesis of handicap signalling to potential insect parasites as an adaptive explanation for autumn leaf colouration. In subsequent studies there has been little attention to the costs and benefits of early autumnal colour change. Yet, in an observational study by Hagen et al. (2003) it was demonstrated that birch trees [Betula pubescens ssp. czerepanovii Ehrhart (Betulaceae)] turning yellow early in autumn had less damage from insects chewing on leaves the subsequent summer. Here, two experiments are presented which test the mechanisms in this model. The first addresses the proposed defence of leaves of B. pubescens ssp. czerepanovii by letting caterpillars of Epirrita autumnata Borkhausen (Lepidoptera: Geometridae), the birches’ most common insect parasites, choose between leaves from trees that either turned yellow late or early the foregoing autumn. The second experiment addresses whether adult female E. autumnata choose between early or late senescent (i.e., yellow or green) ‘twigs’ when ovipositing in autumn. We could not find evidence of preferences in either larvae or females, suggesting that timing of colour change in B. pubescens ssp. czerepanovii is not a warning signal that elicits a response in E. autumnata.