Heliconius melpomene

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

One of the current hot topics in evolutionary biology is to what extent we can predict the genetic path of evolution.

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. Darwin 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 aims to study the predictability of evolution by revealing 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. Work by Dr Chris Jiggins’ group in the Department of Zoology has focused on Heliconius butterflies as a case study in evolutionary biology.

By testing the role of Heliconius wing patterns in the wild, Dr Jiggins and others 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.

Selection signatures

One of the current hot topics in evolutionary biology is to what extent we can predict the genetic 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 new project focusing on the genetic basis of wing patterns has commenced in the Jiggins lab 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 Wellcome Trust Sanger Institute, regions of the butterfly genome are being sequenced to 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 contains 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 ‘hot spots’ 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 that were posed at the very dawn of evolutionary biology. Throughout the intervening decades, 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.

For more information, please contact the author Dr Chris Jiggins (c.jiggins@zoo.cam.ac.uk) at the Department of Zoology.

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