Roz Evans | Masters of masquerade
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Masters of masquerade

In sun-speared woodlands across Asia, odd, aged and mottled oak leaves sit incongruously upon rocks and trunks of trees to which they do not belong. Of interest to no one, a dead leaf provides no sustenance for the creatures that live amongst these trees, perhaps only occasionally looking useful to nesting birds and mammals. But the rustle of nearby undergrowth or a gust of wind sends the old leaves up into the sky, defying gravity. And with flashes of blue, orange and iridescent purples the brittle oak leaves reveal their true identity. These fluttering faux leaves are Kallima butterflies, almost perfectly masquerading as the fallen fingertips of mature oaks – displaying darkened veins, lifeless browns and even fungus spots of real leaves. But unlike them, they are not destined to dry and fade into delicate skeletons. Instead they are able to fly for around six months of the year, seeking suitable places to mate and lay eggs. When a bird or another predator spots a Kallima on the wing, seeing its true colours, pursuit breaks out. In danger of ending its short life at this opportunistic beak, Kallima butterflies drop down into the foliage, close their wings and remain still – becoming once again a dead leaf, appealing to no one, least of all a hungry bird.

Alfred Russell Wallace, one of the leading evolutionary thinkers of the 19th Century, was inspired to travel by Charles Darwin, to whom he dedicated his book ‘The Malay Archipelago’. In this book, Wallace describes how he encountered the Indian leafwing Kallima paralekta, and noted it “the most wonderful and un-doubted case of protective resemblance in a butterfly”. Following this description, biologists from Darwin to modern day evolutionary scientists have argued that the butterflies came to look so strikingly similar to dead leaves through a gradual process of natural selection. At some point, some caterpillars metamorphosed into butterflies with wings that had properties similar to dead leaves, making them slightly less likely to be caught by a bird. These butterflies survived and reproduced, passing on their genes and producing offspring that also slightly resembled dead leaves. Those offspring that resembled dead leaves the most would be the most successful, and so on the process goes until we reach a point today where the resemblance is so striking that we call it ‘masquerade mimicry’.

However, this wasn’t a universally held view. In 1945, when discussing the forefathers of evolution, Richard Goldshmidt stated that “all of these authors and their followers had the feeling, if not the conviction, that a considerable part of the secret of evolution lay hidden behind the manifold and beautiful patterns of Lepidoptera, and that an understanding of these patterns would constitute a large step towards the explanation of evolution.” This was something that evolutionary biologists were in agreement over, but they were not in agreement over the evolutionary mechanisms. Goldshmidt advocated for the sudden emergence of leaf mimicry patterns without intermediate forms. Gradual evolution through natural selection is gradual and therefore generally slow. In the intermediate stages, it is argued that poor mimicry would make an individual more vulnerable to predation, making the full trait hard to develop. Goldshmidt did not believe that the selection of small mutations that warranted the leaf colouration in each generation could lead to the evolution of the Kallima butterflies as we know them.

This conflict has remained unresolved – until now, perhaps.  Researchers from the National Institute of Agrobiological Sciences, Japan have released a paper in the journal BMC Evolutionary Biology,  hoping to provide an answer. “Despite enthusiastic debate, there is as yet no direct experimental evidence” said Takao Suziki, lead author of the paper.

“To reveal the process by which leaf patterns evolved, we focused on the long-term evolution toward leaf mimicry patterns across several hundred species over about 70 millions years,”  explains Takao. The team analysed 47 species of butterfly across 18 genera and determined their genetic relationship to the Kallima butterflies. Then, through a process of statistical analyses they were able to infer what the past pattern states of these 47 species would have been. “To do this inference, we decomposed the butterfly wing patterns into 11 elements and inferred when 11 elements changed in the states and then reconstructed the ancestral wing patterns as an assembly of 11 elements.”

From this, they believe they have shown the evolution through four intermediate patterns. Through further statistical tests they were then able to show how elements of the wing patterns changed over time “finally establishing a close resemblance to a leaf venation-like appearance”.

Takao and his team believe they have proven with their analysis that the intricate leaf patterning of Kallima butterflies did indeed evolve through a gradual process from wings that did not resemble leaves. Unfortunately, the team were unable to investigate how the intermediate forms of the masquerading butterflies were able to survive, so perhaps they would not satisfy the questions of Goldshmidt, but they believe that their results ‘strongly suggest’ that this gradual evolution through intermediate states was indeed the way that these masqueraders came to so perfectly mimic old leaves.

“In the past, leaf mimicry in Kallima butterfly species was a cornerstone in arguments for saltatory evolution, in which context Goldschmidt argued that this mimicry must have originated suddenly as a ‘hopeful monster’, without any intermediate forms. The discovery revealed in this study refutes such claims and demonstrates that the appearance of leaf mimicry in Kallima spp. has arisen in a stepwise and contingent fashion.”

Takao believes that even though there were intermediate states, they still formed an ‘imperfect masquerade’ and instead of the new forms standing out against the crowd of other butterflies, they blended in – somewhat imperfectly – to the fallen leaves and shrubs on the forest floor. In order to really understand how these in-betweeners survived, Takao says that we would look to the foraging behaviour of their predators, and the strategy that the butterflies at that time would have used to escape.

Kallima butterflies are not alone in their masterful masquerading. Could this confirmation of a gradual evolutionary process be true of all of nature’s spurious species?  Employing such incredible masquerade, the latter part of the Satanic leaf-tail gecko’s scientific name Uroplatus phantasticus is the latin for ‘imaginary’ – so unbelievably mythical is its appearance.  Perhaps an even better mimic of dead leaves than the flattened Kallima, its tail and body are curled and mottled into perfectly imperfect dried-up clusters, complete with faux nibble-dents and deterioration. However, Takao hesitates at the idea of explaining the evolution of vertebrate mimics in the same way; “pigmentation systems of vertebrates are largely different from those of insects” and he suggests that it is likely that the evolutionary paths were different.

In contrast, Takao believes it is “far from impossible” to explain other insect mimicry on the basis of their findings. Various species of bolas spider (Mastophora) resemble bird droppings, as well as the aptly named bird-dropping spider, keeping themselves off the menu of their avian predators.  Whilst the bird-dropping bolas spiders spend their time on the upper surface of leaves, the bolas spider M. bisaccata resembles the shell of a snail often found in its habitat, and resides on the underside of leaves – taking the appropriate placing for the subjects they mimic. Unlike most spiders their entire strategy to life is different – not scuttling away on 8 quick legs, but remaining still – inanimate. As the Kallima butterflies might drop down into the leaf litter when threatened, adopting different behavioural strategies to compliment the masquerade can fool the search images of one’s predator. Not only do you look like a leaf, a shell or a bird dropping, but you behave like one too. The walking leaf insect (Phyllium giganteum) does not resemble dead leaves, but green ones full of life. Not only does it look the part, but when it walks it waves from side to side – as if blowing in the wind, just as a real leaf would. Although perhaps succulent looking to a hungry, hungry caterpillar, the insect’s main predators don’t notice it from the other leaves, and go on to look for more obvious juicy insects instead. The name of the game is to appear tasteless to your predators. Along with mantids resembling beautiful orchids, using their disguise to catch unwitting pollinators, and insects garnering their name from the sticks they feign to be, this cohort is masterful – perhaps all slowly, gradually, over countless generations becoming some of nature’s greatest pretenders.

Date

March 27, 2015

Category

Writing