A test of the coevolution theory of autumn colours: colour preference of Rhopalosiphum padi on Prunus padus

According to the coevolution theory of autumn colours, the bright colours of trees evolved as a warning signal towards parasites colonizing the plant in autumn. We monitored colonization of the aphid Rhopalosiphum padi on individual tress of Prunus padus in autumn and observed a strong preference of aphids for trees with green leaves. This is the first direct observation of a key assumption of the theory, that parasites avoid bright colours. Moreover our observations, compared with previous data gathered on the same species, suggest that aphids colonizing trees with green leaves develop better in spring than aphids colonizing trees with bright autumn colours, which is consistent with the second main assumption of the coevolution theory.     

Autumn colours and the nutrient retranslocation hypothesis: a theoretical assessment

The adaptive value of the bright colours of leaves in autumn is still debated. It is possible that autumn colours are an adaptation to protect the tree against photoinibition and photooxidation, which allows a more efficient recovery of nutrients. It has been proposed that the preference of aphids for trees that retranslocate nitrogen more efficiently can explain the high diversity of aphids on tree species with bright autumn colours. This scenario however does not take into account the impact of insects on the fitness of the trees and has not been analysed theoretically. Its assumptions and predictions, therefore, remain uncertain. I show with a model of insect-tree interaction that the system can actually evolve under particular conditions. I discuss the differences with the coevolution theory of autumn colours, available evidence and possible tests.     

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.     

Decoupling vigour and quality in the autumn colours game: Weak individuals can signal, cheating can pay

According to the coevolution theory, autumn colours are a warning signal to insects, signalling the level of chemical defences or availability of nutrients. Because in the original model tree vigour and defences were positively correlated, it is not clear whether signalling would still be stable when they are decoupled, and the fact that weak trees often display bright autumn colours is usually presented as evidence against the coevolution theory. I show that in a theoretical model of insect-tree coevolution, signalling is still stable when vigour and defences are decoupled. Weak trees can signal. Moreover, partial cheating is possible. The different equilibria depend on the importance of vigour and defences against insect attack, of vigour in the production of the signal, and of pleiotropic effects between colour and defences. These results provide precise predictions that can be used for planning future empirical test.     

Do autumn leaf colours serve as a reproductive insurance against sucking herbivores?

Although autumn leaf colours of deciduous trees have been shown to protect against photo-oxidative damage, they are sometimes seen as signals to pests and predators. Here I modify the coevolution hypothesis of autumn leaf colours. I suggest that much of the within-population variation in autumn leaf colours can be explained by differences in the allocation of resources to sexual reproduction. According to the novel hypothesis, reproductively active woody plants produce early and intense autumn leaf colours in order to protect seeds and other reproductive tissues from pests that lay eggs in the autumn. If many seeds mature at times of leaf senescence or during the next summer, a woody plant will reallocate plenty of nitrogen to seeds. If sucking insects reproduce on such hosts, their flightless offspring will suffer poor-quality food after the ripening of seeds. Before this, however, insects will probably concentrate around the ripening seeds to forage on nitrogen-rich veins. This will decline the quality and quantity of developing seeds. If, on the other hand, insects are able to recognize reproductively active plants while laying eggs in the autumn, both the insects and the plants benefit. The flightless offspring of insects feeds on plants that supply sufficiently nitrogen for longer than reproducing plants do, while these optimise their reproduction by avoiding pests, which also contributes to the abundance of specialist pests. Hence, I suppose that while physiological factors are the origin of autumnal colour changes of deciduous leaves, the visible cue utilized by insects has evolved several times to an honest signal that reveals the unsuitability of the potential host in the near future. The reproductive insurance hypothesis may help us to understand why bright autumn leaf colours are rare among herbaceous plants, and why plants at high altitudes and latitudes are often brightly coloured in autumn.     

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.     

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.     

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.     

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.     

The adaptive significance of autumn leaf colours

Recently W.D. Hamilton and colleagues proposed a provocative new theory to explain the adaptive significance of autumnal leaf colours. They suggested that these colours were signals produced by the trees to warn potential insect herbivores of their defensive ability and tested this theory by an analysis of data on aphid species richness on different tree species. Here we argue that the principal assumptions of their theory do not match current knowledge of plant pigment biochemistry and aphid ecology. We therefore present further adaptive explanations for autumn leaf colours and suggest alternative reasons for the reported relationship between tree leaf colour and aphid species richness.     

Autumn coloration as a signal of tree condition

Hamilton and Brown suggested that bright autumn coloration in trees is an energetically expensive and therefore honest (handicap) signal of defensive commitment against insects. If this is so, one should expect that the intensity of the proposed signal should depend strongly on tree health. However, to the best of our knowledge, the link between vigour and autumn colour has never been tested. We explored the relationship between autumn coloration and tree condition (i.e. leaf fluctuating asymmetry) in mountain birch (Betula pubescens). Our results indicate that bright autumn birches are in better condition and therefore consequently should be better at combating herbivores.     

Genotypic variation in yellow autumn leaf colours explains aphid load in silver birch

? It has been suggested that autumn-migrating insects drive the evolution of autumn leaf colours. However, evidence of genetic variation in autumn leaf colours in natural tree populations and the link between the genetic variation and herbivore abundances has been lacking. ? Here, we measured the size of the whole aphid community and the development of green-yellow leaf colours in six replicate trees of 19 silver birch (Betula pendula) genotypes at the beginning, in the middle and at the end of autumn colouration. We also calculated the difference between green leaf and leaf litter nitrogen (N) and estimated the changes in phloem sap N loading. ? Autumn leaf colouration had significant genetic variation. During the last survey, genotypes that expressed the strongest leaf reflectance 2-4 wk earlier had an abundance of egg-laying Euceraphis betulae females. Surprisingly, the aphid community size during the first surveys explained N loss by the litter of different birch genotypes. ? Our results are the first evidence at the tree intrapopulation genotypic level that autumn-migrating pests have the potential to drive the evolution of autumn leaf colours. They also stress the importance of recognizing the role of late-season tree-insect interactions in the evolution of herbivory resistance.     

A field study with geometrid moths to test the coevolution hypothesis of red autumn colours in deciduous trees

Red autumn colouration of trees is the result of newly synthesized anthocyanin pigments in senescing autumn leaves. As anthocyanin accumulation is costly and the trait is not present in all species, anthocyanins must have an adaptive significance in autumn leaves. According to the coevolution hypothesis of autumn colours, red autumn leaves warn herbivorous insects – especially aphids that migrate to reproduce in trees in the autumn – that the tree will not be a suitable host for their offspring in spring due to a high level of chemical defence or lack of nutrients. The signalling allows trees to avoid herbivores and herbivores to choose better host trees. In this study the coevolution hypothesis was tested with four deciduous tree species that have red autumn leaf colouration – European aspen (Populus tremula L.) (Salicaceae), rowan (Sorbus aucuparia L.) (Rosaceae), mountain birch [Betula pubescens ssp. czerepanovii (NI Orlova) Hämet‐Ahti], and dwarf birch (Betula nana L.) (Betulaceae), and with two generalist herbivores, the autumnal moth [Epirrita autumnata (Borkhausen)] and the winter moth [Operophtera brumata (L.)] (both Lepidoptera: Geometridae). Anthocyanin concentrations of autumn leaves were determined from leaf samples and the growth performance parameters of the moth larvae on the study trees were measured in the spring. Trees with higher anthocyanin concentration in the autumn were predicted to be low‐quality food for the herbivores. Our results clearly showed that anthocyanin concentration was not correlated with the growth performance of the moths in any of the studied tree species. Thus, our study does not support the coevolution hypothesis of autumn colours.     

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.     

Red reveals branch die-back in Norway maple Acer platanoides

Background and Aims

Physiological data suggest that autumn leaf colours of deciduous trees are adaptations to environmental stress. Recently, the evolution of autumn colouration has been linked to tree condition and defence. Most current hypotheses presume that autumn colours vary between tree individuals. This study was designed to test if within-tree variation should be taken into account in experimental and theoretical research on autumn colouration.

Methods

Distribution of red autumn leaf colours was compared between partially dead and vigorous specimens of Norway maple (Acer platanoides) in a 3-year study. In August, the amount of reddish foliage was estimated in pairs of partially dead and control trees. Within-tree variation in the distribution of reddish leaves was evaluated. Leaf nitrogen and carbon concentrations were analysed.

Key Results

Reddish leaf colours were more frequent in partially dead trees than in control trees. Reddish leaves were evenly distributed in control trees, while patchiness of red leaf pigments was pronounced in partially dead trees. Large patches of red leaves were found beneath or next to dead tree parts. These patches reoccurred every year. Leaf nitrogen concentration was lower in reddish than in green leaves but the phenomenon seemed similar in both partially dead and control trees.

Conclusions

The results suggest that red leaf colouration and branch condition are interrelated in Norway maple. Early reddish colours may be used as an indication of leaf nitrogen and carbon levels but not as an indication of tree condition. Studies that concentrate on entire trees may not operate at an optimal level to detect the evolutionary mechanisms behind autumnal leaf colour variation.Key words: Acer platanoides, Norway maple, branch die-back, coevolution hypothesis, leaf senescence, patchy distribution, red leaf pigments, tree condition, within-tree variation     

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.     

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.     

Insect colour preference compared to flower colours in the Australian Alps

An apparent predominance of plant taxa with pale flowers in the alpine floras of Australia and New Zealand may be due to the prevalence of insects, such as flies, that prefer pale colours and the absence of other types of potential pollinators that are attracted to bright colours such as social bees and birds. In this study, the diversity of flower colours, and the preference of insects for different colours were examined for the largest contiguous alpine area in Australia, around Mt Kosciuszko. Out of an alpine flora of 204 taxa, 127 species were found to have large showy flowers. The most common flower colour among these taxa was white (53.5%), then yellow (21.3%), followed by pink (6.3%), and cream (6.3%). Only a handful of taxa had red, blue, brown, green, orange or purple flowers. When the colour preference of insects was tested using five different coloured traps (white, yellow, orange, red and purple), the most successful traps were white then yellow, with these two colours accounting for 66% of all individual insects collected. Diptera were the most common insects caught (576 insects greater than 4 mm in length, 31 morphotaxa) showing an apparent preference for white and yellow coloured traps over others. Therefore, the results add some support to the proposition that the 'white' flora of the Australian Alps may be associated with the colour preference of flies, which have previously been found to be the most common type of pollinators in the Kosciuszko alpine zone.     

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.     

Red leaves, insects and coevolution: a red herring?

W.D. (Bill) Hamilton proposed that coevolution between plants and herbivorous insects explains the bright autumnal colouration of leaves. Accordingly, plants invest in bright signals to reduce their herbivore load, whereas insects use these bright signals to identify less-defended hosts more efficiently. Archetti and Brown have recently revisited this theory by explaining its basic predictions and providing new research perspectives. Their work presents an important basis to our understanding of non-green leaf colouration, provided that alternative adaptive explanations on the photoprotective and antioxidant role of leaf pigments, or their possible function in crypsis to herbivores are incorporated into future research.