On the wings of a butterfly

Since Darwin’s time, Amazonian butterflies have fascinated evolutionary biologists as examples of evolution in action.

On reading Henry Walter Bates’ 1862 account of his travels in the Amazon, Charles Darwin was captivated not only by Bates’ description of the stunning diversity of butterfly species and wing patterns found in the Amazonian jungle, but also by the impressive mimicry between unrelated species. He wrote: ‘It is hardly an exaggeration to say, that whilst reading and reflecting on the various facts given in this Memoir, we feel to be as near witnesses, as we can ever hope to be, of the creation of a new species on this earth.’1

Bates hypothesised that mimicry evolved to confuse predators. Edible butterflies, for instance, copied the wing patterns of toxic species so that predators would avoid eating them. He also described what looked like evolution in action: he observed a continuum, from variable species, in which different wing patterns were found together in the same locality, through to related species with different wing patterns. Now, 150 years later, modern science has taken this to another level, with new research that attempts to uncover the genetic predictability of evolution by identifying the genetic basis of wing pattern mimicry.

The importance of pattern

We now recognise that not only do edible species mimic nasty ones (today called Batesian mimicry), but that several nasty species can also benefit from mimicking one another (Müllerian mimicry) – bees and wasps being a familiar example. Many of the Amazonian butterflies described by Bates are in fact Müllerian mimics, and the best-studied group are the genus Heliconius, the passion vine butterflies. Recent work has focused on the Heliconius butterflies as a case study in evolutionary biology.

Studies of Heliconius wing patterns in the wild have confirmed Bates’ hunch: changes in wing pattern play a big role in determining how successful the butterflies are in both mating and avoiding being eaten. Using flapping models with different patterns, the researchers have shown that the butterflies choose to mate with individuals that look the same as themselves; because of this, over time, different patterns are likely to split into new species. In addition, hybrids between populations with different patterns have intermediate patterns that are not recognised by predators as harmful and therefore suffer disproportionately from attacks, reinforcing the split into new species.

This dual role of wing patterns in signalling both to predators and to potential mates makes pattern a ‘key trait’ for speciation. As Bates suggested, shifts in wing patterns do indeed lead to the evolution of new species.

Signatures of selection

One of the current hot topics in evolutionary biology is to what extent we can predict the path of evolution. One particular Heliconius species (Heliconius melpomene) is an ideal system in which to address this question because it has many geographic populations with very different colour patterns. A major collaborative project focusing on the genetic basis of wing patterns is underway with funding from the Biotechnology and Biological Sciences Research Council (BBSRC), Royal Society, Leverhulme Trust and Natural Environment Research Council (NERC).

Over the past decade, the researchers have been collecting different forms of H. melpomene from around South America, carrying out genetic crosses at a field station in Panama. These crosses have shown that dramatic differences in colour pattern are controlled by just a handful of genes, and that these genes are clustered together on four out of the 21 Heliconius chromosomes. The genes act as wing pattern ‘switches’, turning on and off the presence of major pattern elements, such as a large red forewing band. The challenge is to find out precisely what these genes are and how they work.

In collaboration with the Welcome Trust Sanger Institute, regions of the butterfly genome are being sequenced to try and identify the specific nature of the pattern switches. The expectation was that the switches would correspond to well-known genes, perhaps controlling wing development or colour pigments. In fact the two genomic regions studied so far each contain around 20 genes none of which is known for its involvement in these processes. This is in itself exciting as it implies that novel mechanisms of pattern determination are operating; current research is focused on determining which, of all these genes, are having an effect in the butterfly.

Genetics of mimicry

What attracted Darwin and others to mimicry as a case study in evolution is its repeatability – the same patterns evolve in distantly related species. A key question for an evolutionary geneticist is therefore whether the patterns are generated by the same genetic mechanisms, or different ones. Again, Heliconius butterflies are a good system to study this.

Heliconius melpomene co-mimics another species, Heliconius erato, all over the neotropics – in any location you care to look you will find that the two species have evolved identical patterns. Recently, in collaboration with research groups in the USA, it has been shown that pattern switches in the two species are controlled by the same regions of DNA, such that genes at identical locations in the genome code for either a red forewing band or a yellow hindwing bar. This implies that evolution of the same mimicry patterns in the two species has been made easier by a shared genetic system. While predation against abnormal wing patterns drives the evolution of mimicry through Darwinian natural selection, a shared developmental system may bias the raw materials in favour of certain kinds of patterns.

Of course, the link between wing pattern adaptation and speciation requires changes in behaviour. The mating preferences of divergent populations need to evolve in order to match their wing patterns. Remarkably, crossing experiments currently being carried out in Panama show that the genes underlying these changes in behaviour are closely associated with colour pattern genes. It seems that there are ‘hotspots’ in the genome for evolutionary change, influencing traits as diverse as wing patterns and mating preference.

An enduring example

It is an exciting time to be studying butterfly mimicry. The combination of population genetic, developmental and behavioural approaches is starting to answer the issues Darwin and Bates themselves debated; questions which were posed at the very dawn of evolutionary biology. Over the last 150 years, Heliconius butterflies have persisted as an example of evolution in action. With the imminent sequencing of the Heliconius melpomene genome, they will no doubt continue to be so for some time yet. Charles Darwin would surely have approved.

1[Darwin, C.R.] 1863. [Review of] Contributions to an insect fauna of the Amazon Valley. By Henry Walter Bates, Esq. Transact. Linnean Soc. Vol. XXIII. 1862, p. 495. Natural History Review 3: 219–224.

Thanks to those in my lab who helped with the text, Laura Ferguson in particular.  If anyone is interested in reading more about the idea of genomic ‘hotpots’ for evolution, there is a nice recent review of the evidence in Heliconius by Riccardo Papa and others, and a more general overview in Science magazine.

Another of the winners was Nick Barton, who also worked with Jim on Heliconius hybrid zones in the late 1980′s when they were both at UCL (Jim was a postdoc with Nick).  Apparently, Nick visited Tarapoto, Peru during the fieldwork – after months of carrying butterflies across treacherous terrain for release on the other side of the hybrid zone, Jim was getting depressed at lack of progress (a familiar feeling to anyone who has spent long periods in the field). Nick turned up and did a quick likelihood calculation on the back of an envelope to show that the mark-release-recapture experiment was showing significant selection and all was well.  In those days Tarapoto was a pretty remote place…

Anyway, if you want to know more about the linnean society medals, have a look at their press release.

Winners of the Darwin-Wallace Medal, 2009

Plate I of Bates' "heliconid" paper. The handwritten notes are by Alfred Russel Wallace, as this was photographed from Wallace's own copy of the paper

However, Darwin (1863) did comment on Henry Walter Bates’ 1862 paper “Contribution to an Insect Fauna of the Amazon Valley,” although he seems to have confined his comments to what Bates called the “danaoid heliconids” (today’s Ithomiinae) as opposed to the “acraeoid heliconids” (today’s Heliconiina). Darwin was clearly a bit put out that Bates seems to have titled his now famous paper with such a lack-lustre title: “… this memoir, which from its unpretending and somewhat indefinite title we fear may be overlooked in the ever-flowing rush of scientific literature.”

Darwin, today known more for his for “turgid” writing than purple prose, pulls out some superlatives to advertise Bates’ paper: “In these facts, of which only a brief abstract is given, we have the most striking case ever recorded of what naturalists call analogical resemblance. … Why then, we are naturally eager to know, has one butterfly or moth so often assumed the dress of another quite distinct form; why to the perplexity of naturalists has Nature condescended to the tricks of the stage?”

“Mr. Bates has given to these facts the requisite touch of genius, and hs, we cannot doubt, hit on the final cause of all this mimicry. … The mocked and common forms must habitually escape to a large extent, destruction, otherwise they could not exist in such swarms; and Mr. Bates never saw them preyed on by birds … he suspects that this immunity is owing to a peculiar and offensive odour … The mocking forms, on the other hand, … are comparatively rare, [and] must suffer habitually from some danger. … Now if a member of one of these persecuted and rare groups were to assume a dress so like that of a well-protected species … it would often deceive predacious birds and insects, and thus escape entire annihilation. This we believe is the true explanation of all this mockery.”

However, Darwin is most excited by a discussion of Mechanitis in which Bates suggests assortative mating by colour pattern. “We will notice only briefly one other point which has an important bearing on the production of new races and species; namely the statement repeatedly made that in certain cases the individuals of the same variety evince a strong predilection to pair together.” However, Darwin adds: “… we are by our profession as critics bound to be sceptical, and we think that Mr. Bates ought to have given more copious evidence. He ought also to have given in every case his reasons in full for believing that the closely allied and co-existing forms, with which his varieties do not pair, are not distinct species. Naturalists should always bear in mind such cases as those of our own willow wrens, two of which [i.e. willow warbler and chiff-chaff] are so closely alike that experienced ornithologists can with difficulty [scarcely] distinguish them …; yet these are certainly as distinct species as any in the world.

Today’s work with Heliconius does indeed suggest that mimicry evolution entails a coevolved change in mate choice by males, leading to assortative mating in many cases of interracial and interspecies choice tests. Darwin hit on one of the most interesting points in Bates’ memoir, and delivered Bates with a challenge that he, having already returned from the Amazon for the last time, could not fulfil: to get more data on the relationship of the evolution of mimicry to the origin of species.