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Consortium Meeting

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This is to announce that there will be a meeting of the Consortium on July 12-13 in Cambridge Mass. organised by Jim Mallet. Please contact Jim if you would like to attend.

This will be the first meeting since we published the genome paper last year, and the goal is to start the ball rolling for the future – in particular which genomes should we sequence next, how will we deal with databasing and data sharing issues in the era of multiple genomes, and in general to promote discussion about ongoing projects in all the Heliconius labs.

Mimicry among Heliconius biologists

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It has recently been remarked that the phnomenon of mimicry extends to the biologists that study Heliconius. It remains unclear whether this convergence at a phenotypic level involves a common genetic basis. Here are a few examples.

Patricio_Arnaud

Patricio Salazar, who works on hybrid zones and hybridisation and Arnaud Martin, who works with the evolutionary developmental biology of wing patterns.

bob wallbank_cropRobert Reed, Professor at Cornell working on many aspects of Heliconius biology, and Richard Wallbank, recently recruited to butterflies from the world of the fruit fly.

willmott nieldAnd finally, Keith Willmott, author of upcoming Butterflies of Ecuador, and Andrew Nield, author of the Butterflies of Venezuela.

Suggestions for any more instances of this phenomenon would be gratefully accepted.

 

 

Introgression: Brower’s criticisms. Part I.

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New evidence for hybridization and introgression is unsettling

The idea that hybridization and introgression among species occurs and may be evolutionarily important has long been acceptable to botanists: in plants clear examples of hybridization and introgression existed before the advent of molecular genetics. The base of the whole tree of life is now known to be much more like a web than a tree, due to abundant horizontal transfer among prokaryotes. However, such ideas have found little favour with zoologists until recently.

Advances in science can be unsettling. They can be fought against, sometimes irrationally, by those seeking to uphold the status quo ante. Many evolutionary biologists either think that species are “reproductively isolated,” or adhere to phylogenetic or cladistic species concepts with underlying assumptions that deny reticulation since speciation. Hybridization and the possibility that genes might often flow (or ‘introgress’) between species challenge these modes of thought. To those with such convictions, introgression is only rarely involved in adaptive evolution or speciation.

Such feelings still exist among many fellow evolutionary biologists. In the last year, I’ve visited different universities around the USA and discussed recent genomic evidence for introgression in Heliconius butterflies. Many people have commented after my talks that they find the whole idea of such leaky species in animals disturbing.

Heliconius is not the only animal group to show introgression: a variety of other groups such as Darwin’s finches, cichlid fish, Littorina winkles, and among insects Rhagoletis, Zeiraphera, the Drosophila pseudoobscura-persimilis species pair, Hawaiian Drosophila, and Timema, have all lent support to the idea that species boundaries are weaker than we thought even 10 years ago. Increasingly, reviews by Michael Arnold and others have suggested that regular patterns of hybridization and introgression are much more likely than we used to think, especially among recently derived radiations of species. But Heliconius is maybe one of the icons of these new ideas.

Andrew Brower knows the genus Heliconius as well as many of us. Nonetheless, he has recently voiced extreme skepticism to our work in two recent diatribes (Brower 2011, 2012). Brower is disturbed by all this new evidence upending his view of species. As he points out, “… if [homoploid hybrid speciation] has occurred multiple times just within this charismatic genus of butterflies, then speciation theory would seem to be headed for a paradigm shift.”

It would be interesting to know the history of Brower’s 2012 article, and what the reviewers said about it. The article was slipped into the “Reviews” section of the main biological journal of the Royal Society of London, essentially the journal in which Isaac Newton published. Beneath a modest title and apparently neutral abstract, the article is not a balanced review at all. It contains a detailed, point-by-point dismissal of much Heliconius genetic and evolutionary work done by many different laboratories worldwide (except his own) over the last 20 years.

I may have unwittingly triggered Brower’s 2012 article by my reaction to his 2011 piece. I wrote him a personal email, outlining some of the many errors he had made. Undaunted, he has aired a revised set of his views in public, and presumably would like any new errors he has made to be made public also. In this and the next post, I shall attempt to do this.

First, let’s briefly survey evidence for natural hybridization and introgression among species of heliconiine butterflies, that it can lead to the sharing of adaptive colour patterns used in Müllerian mimicry, and that it is involved in speciation. Then we can discuss whether Brower’s critiques have any validity (in the next post).

I take his criticisms personally because the conclusions attacked refer to many major findings of our group since the 1990s, and to the findings of a number of ex-students and ex-postdocs.

I also take this personally because Brower helped to sabotage in 2001 an earlier attempt to publish details of hybrid specimens. The data was documented from museums and private collections worldwide, and had been gathered since the mid-1990s. Brower’s signed review helped to prevent publication of the data set until the late 2000s (Mallet et al. 2007). A major argument he used then, and which he still does against the same data set, is you can’t trust museum specimens: they are either fraudulent or misinterpreted. (Another argument he used then was that in any case they aren’t hybrids at all, but he seems to have dropped that particular idea for now). Even if some of the many specimens in the data set are fraudulent (unlikely, and anyway a possibility discussed carefully in the original paper), and even if he didn’t like the conclusions, it seems to me that to use these grounds to suppress detailed documentation of these interesting hybrids was inexcusable.

Evidence for hybridization, introgression and hybrid speciation in Heliconius

1) Hybridization in nature. Hybrids between Heliconius species in nature are usually common on a per species basis (Mallet et al. 2007), although rare on a per individual basis (mostly less that 1 in 1000 individuals of any species). As well as F1 crosses, F2 and backcross phenotypes are produced in nature. F1 females are usually sterile, but F1 males can be used in backcrosses. This applies to the whole melpomene-silvaniform group, within which it is possible to cross and backcross, enabling transfer of colour patterns in the laboratory, across that whole group of ~15 species (see suppl. info. in Mallet et al. 2007).

These facts alone suggest that some genes must flow between species, and that, although many loci may find themselves to be incompatible, it would not be surprising that sometimes transferred genes or groups of genes can be advantageous in their new contexts. Although hybridization at a rate of 1/1,000 or 1/10,000 seems rare, it would still be much more important than mutation in introducing new variants into populations. When multilocus adaptations are involved, which have already been tested within one species, the importance of (multi-)gene flow could be even greater.

2) Evidence from gene flow using Isolation-Migration (IM) coalescent algorithms. Coalescent analyses of small numbers of some (but not all) loci sequenced using traditional PCR-Sanger methods suggest gene flow between cydno, melpomene, and related Heliconius (Bull et al. 2006, Kronforst et al. 2006, Mavárez et al. 2006, Kronforst 2008).

3) Heliconius heurippa — a hybrid species. The colour pattern of a putative hybrid species, Heliconius heurippa, can be produced in the laboratory via crosses between Heliconius cydno cordula and H. melpomene melpomene, which overlap nearby. Heliconius heurippa appears to be a cydno-lineage species that obtained its red forewing colour pattern and underside markings from the H. melpomene with which it still overlaps (Mavárez et al. 2006).

Populations of H. cydno cordula and H. melpomene melpomene overlap a few tens of km to the North, in San Cristóbal, Venezuela. This population shows abundant evidence of past hybridization, with some specimens of melpomene having polymorphic colour pattern elements from cydno, and some specimens of cydno showing polymorphic elements of melpomene (Mallet & Mavárez 2003, Mavárez et al. 2006).

Bizarrely, Brower interpreted  a single specimen from among these polymorphic forms in San Cristóbal as a new species in the cydno/timareta species group (Brower 2012, Fig. 1.14), but this is surely a very unparsimonious idea, given the multiple other hybrid phenotypes also present at the site (Mallet & Mavárez 2003). This Venezuelan site thus provides exactly the sort of intermediate hybrid population (i.e. a red-banded colour polymorphism in cydno) required as a first step towards establishment of a fixed red-banded hybrid taxon, such as H. heurippa (Mavárez et al. 2006).

An earlier critique of the hybridization hypothesis by Michael Turelli & Jerry Coyne was submitted to Nature, but unfortunately, in my view, remained unpublished. Nonetheless I still believe that the Mavárez et al. paper had the correct interpretation. The most parsimonious explanation is that the colour pattern of H. heurippa was obtained via a cross between a yellow banded cydno and a red-banded melpomene. H. heurippa and H. melpomene continue to hybridize occasionally; I have examined a wild-caught hybrid (Mallet et al. 2007, no. 97). The most suitable races of each parental species to produce the heurippa phenotype are also those that happen to overlap or nearly overlap currently with heurippa. The Turelli & Coyne critique didn’t really address the central idea that the unique colour pattern of H. heurippa is parsimoniously explained as a hybrid between colour patterns which occur locally.

Camilo Salazar later published a paper suggesting, on the base of extensive sequencing, that introgression of colour pattern in H. heurippa involved the gene kinesin (Salazar et al. 2010). Kinesin is now known to be very close to, but is probably not at the actual location of the colour pattern regulatory switches, which seem largely to affect the expression of optix in the pupal wing (Reed et al. 2011, Heliconius Genome Consortium 2012, Pardo-Diaz et al. 2012).

Personally, I thought that the Coyne & Turelli critique missed something they could have argued. This was not that hybridization was not involved in the origin of heurippa‘s colour pattern (it likely was), but that the resultant taxon may not be a “good” species since it is not known to overlap with one of its putative parents. H. cydno cordula occurs nearby, but only at a small distance North of the known range of H. heurippa on the Eastern slopes of the Andes. H. heurippa might then be only a geographic race or “semispecies” of the cydno/timareta superspecies. Guerilla activity has hitherto prohibited exploration of the probable contact zone between heurippa and this cydno race, near Yopal, Colombia. Nonetheless, Camilo Salazar in Mavárez et al. (2006) showed, using courtship tests, that heurippa is partially reproductively isolated from both parents by its hybrid colour pattern, and therefore that one could justify the species label on that ground. As pointed out elsewhere, similar critiques of non-overlap of parental and offspring hybrid taxa could be levelled against most other animal or plant examples of homoploid hybrid species; they too overlap only rarely with both putative parents (Mallet 2007). A recently revealed exception to this pattern is Heliconius elevatus, which overlaps extensively with both putative parents H. pardalinus and H. melpomene across the entire Amazon basin (Heliconius Genome Consortium 2012, and see point (6) below).

Next-generation genomic studies have strengthened these preliminary forays, and reveal even more evidence for “promiscuous” gene flow than we thought.

4) RAD resequencing across the whole genome. Where “postman-patterned” H. timareta overlaps with “postman-patterned” H. melpomene in NE Peru, so-called ABBA-BABA nucleotide sites in RAD tags show genome-wide evidence of flux (excess of ABBA sites over BABA sites) across the species boundary (NB, timareta is another member of the cydno group lineage) (see part (b) of Fig. 1 below. The adjacent “rayed” race of H. melpomene used as a control, which does not overlap with H. timareta in Peru, shows virtually no ABBA-BABA excess. This provides critical evidence as the races of H. melpomene are separated by only a few tens of km across a narrow hybrid zone, and the Fst between postman and rayed melpomene is minuscule, as expected for spatial structuring at this geographic distance (Heliconius Genome Consortium 2012).

Figure on genome wide D-statistics

Fig. 1. D-statistics across the genome. a, ABBA and BABA nucleotide sites employed in the test are derived (– – B –) in H. timareta compared with the silvaniform outgroup (– – – A), but differ among H. melpomene amaryllis and H. melpomene aglaope (either ABBA or BABA). As this almost exclusively restricts attention to sites polymorphic in the ancestor of H. timareta and H. melpomene, equal numbers of ABBA and BABA sites are expected under a null hypothesis of no introgression, as depicted in the two gene genealogies. b, Distribution among chromosomes of Patterson’s D-statistic (±s.e.), which measures excess of ABBA sites over BABA sites, here for the comparison: H. m. aglaope, H. m. amaryllis, H. timareta ssp. nov., silvaniform. Chromosomes containing the two colour-pattern regions (B/D, red; N/Yb, yellow) have the two highest D-statistics; the combinatorial probability of this occurring by chance is 0.005. The excess of ABBA sites (0 < D < 1) indicates introgression between sympatric H. timareta and H. m. amaryllis. (Fig. 3, from Heliconius Genome Consortium 2012)

 

The excess of ABBAs over BABAs used to infer gene flow is hard to explain by pre-existing population structure, which was one of Graham Coop’s suggestions (Coop 2012), because the local genome-wide bias exists right across many chromosomes in two species both of which have much broader distributions. Coop suggested also that this effect might be due to alignment bias. This sounds reasonable, because the alignments used a postman H. melpomene melpomene from Panama as a genomic reference sequence. But it is unlikely to be the explanation because we’re here comparing races in Peru that  are much closer (smaller Fst) than either is to H. melpomene melpomene from Panama. There’s therefore no reason to expect a bias across the whole genome to just one of this pair of races Amazonian races, as found.

5) Sureselect resequencing of colour pattern regions. Fixed ABBA-BABA sites in colour pattern regions show extremely strong, in fact the genome-wide strongest, evidence for gene flow both between the Peruvian postman forms of melpomene and timareta, and also between Colombian rayed forms of melpomene and timareta (Heliconius Genome Consortium 2012). This reciprocal evidence for transfer, in exactly the expected direction(See (b) and (c) in Fig. 2 below), and almost exclusively within colour pattern divergence peaks (Fig. 2a, below) between the aforementioned races that meet in Peru, seems to us convincing evidence that colour patterns were transferred .

Graham Coop (Coop 2012), and Michael Turelli (question after a seminar, UC Davis in November 2012) have both suggested that this might instead be caused by ancestral population structure. But it’s hard to know how. This might happen, I suppose, if timareta speciated from melpomene “multiregionally,” so that each species inherited some of the same multiple, locally fixed colour patterns from their widespread and polytypic common ancestor. The need for this unknown mode of speciation is avoided, however, if gene flow among species takes place. There is already genome-wide evidence for polymorphic transfers (see (4) above). Therefore, exchanges of colour pattern regions will also take place from time to time. Then occasional fixation of such introduced ~10-50 kb colour-pattern determining genomic regions seems not at all improbable, given the kinds of mimetic selection expected.

ABBA-BABA graphs

Fig. 2. ABBA-BABA and phylogenetic evidence of introgression at the B/D colour pattern locus. a, Genetic divergence between H. melpomene races aglaope (rayed) and amaryllis (postman) across a hybrid zone in northeast Peru. Divergence, Fst, is measured along the B/D region (Supplementary Information 14) and peaks in the region known to control red wing pattern elements between the genes kinesin and optix. b, c, Distribution of fixed ABBA and BABA sites (see Fig. 3a) along B/D for two comparisons. Excesses of ABBA in b and BABA in c are highly significant (two-tailed Z-tests for D = 0; D = 0.90 ± 0.13, P = 5 × 10^−14 and D = −0.91 ± 0.10, P = 9 × 10^−24, respectively), indicating introgression. d, e, f, Genealogical change along B/D investigated with maximum likelihood based on 50-kb windows. Three representative tree topologies are shown. Topology A, [approximately] the ‘[true] species tree,’ is found within the white windows. In topologies B (dark green window) and C (light green windows) taxa group by colour pattern rather than by species. Within striped windows, H. melpomene and/or H. timareta are paraphyletic but the taxa do not group by colour pattern. Support is shown for nodes with >50% bootstrap support. (Fig. 4 from Heliconius Genome Consortium 2012).

 

6) Sureselect resequencing of colour pattern regions, contd. Resequencing also yielded phylogenetic evidence for wholesale transfer of two melpomene ray-pattern genomic regions to a Heliconius pardalinus-like ancestor of Heliconius elevatus (Fig. 2d, above), giving a very recently formed rayed species that, according to the rest of its genome is in fact nested within H. pardalinus (Heliconius Genome Consortium 2012). H. elevatus, together with its two putative parent species, today coexist in widespread sympatry throughout the Amazon basin. We hypothesise that this represents a hybrid speciation event triggered, at least in part, by the acquisition of this rayed colour pattern, which is unique among the ~9 spp. of the “silvaniform” group of Heliconius.

7) Whole genome resequencing. What we lacked in the Genome Consortium paper was a genome-wide RAD analysis of ABBA-BABA sites of the Colombian populations of timareta and melpomene, to match the SureSelect data from the colour pattern genomic regions. For the Peruvian populations we had both sets of data. The lack of a reciprocal design came about because the colour pattern data from Colombian timareta were added as an afterthought to the genome paper.

It seems worth mentioning that we’ve now carried out a reciprocal genome-wide analysis of the sort indicated. We used populations of cydno and melpomene in Panama (where the two are not mimetic, and did not exchange colour patterns), and of timareta and melpomene in Peru (where it is argued the two species have exchanged colour patterns). This time, instead of using RADs, we have Illumina whole genome sequence data to ~30-40x, for each of 4 individuals for each species and site. These intriguing new data suggest the exchange of very large fractions of the genome at both sites. This reciprocal whole-genome evidence from two sites provides very strong evidence for abundant genetic transfer in localities where Heliconius melpomene overlaps with H. cydno and H. timareta (Simon Martin et al., submitted).

Brower’s critique and its refutation

Faced with such a mountain of evidence, Brower has an uphill task to perform. The case for hybridization and introgression seems solid because dismantling any one piece of evidence does not cause the whole argument to fail. Undaunted, Brower proceeds to attack every single data item and inference that points to the foregoing conclusions. If Brower is correct, many separate workers across the world have conspired to slant their conclusions towards an idea for which there is, in fact, no evidence at all, according to Brower.

In the next post I’ll enumerate Brower’s criticisms and discuss them individually.

Part II: http://www.heliconius.org/2013/introgression-browers-criticisms-part-ii/

Brower AVZ. 2011. Genetica 138: 589.
Brower AVZ. 2012. Proc Roy Soc B 280 online.
Bull V et al. 2006. BMC Biol 4: 11.
Coop G. 2012. http://gcbias.org/2012/05/23/journal-tea-may-21st/
Heliconius Genome Consortium. 2012. Nature 487: 94.
Kronforst MR. 2008. BMC Evol Biol 8: 98.
Kronforst MR et al. 2006. Evolution 60: 1254.
Mallet J. 2007. Nature 446: 279.
Mallet J & Mavárez J. 2003. (In Mallet et al. 2007). See: http://www.biomedcentral.com/content/supplementary/1471-2148-7-28-s1/mavarez/cristobaltab.html
Mallet J et al. 2007. BMC Evol Biol 7: 28.
Mavárez J et al. 2006. Nature 441: 868.
Pardo-Diaz C et al. 2012. PLoS Genet 8: e1002752.
Reed RJ et al. 2011. Science 333: 1137.
Salazar C et al. 2010. PLoS Genet 6: e1000930.

Genome sequence published!

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Our Heliconius Genome Consortium paper was just published in Nature describing the genome sequence of Heliconius melpomene. As well as being a fantastic resource for all sorts of future studies, in the paper we used the genome to show that mimetic Heliconius can converge by exchanging genes through hybridization. Its not just Heliconius heurippa – hybridization is happening all over the place…

Here is the press release:

An international collaborative study to map the genome of a South American butterfly has identified the secret behind its mimetic nature.

The genome sequence of the Postman butterfly, Heliconius melpomene, was used as a reference to study species that live together in the Peruvian Amazon. Several of these share bright wing patterns in order to reinforce a warning signal that they are bad to eat – dissuading predators from attack.

Sequence data showed that those species with similar wing patterns shared a similar genetic signal, precisely in those narrow regions of the genome responsible for controlling patterns. This is a result of hybrid exchange of genes between three co-mimic species, which has allowed them to copy each other’s wing patterns.

Dr Chris Jiggins of the University of Cambridge said, “These butterflies, in order to better survive in the wild, have taken successful survival techniques from other butterflies and have incorporated them into their own genetic code. This is significant as it has occurred in a natural adaptive radiation, suggesting an important role for hybrids in the origins of biodiversity.”

The phenomenon, known as adaptive introgression, involves different species sharing genetic material and has been considered very rare, especially in animals. Although many species can interbreed in the wild, the resulting hybrids are often infertile and considered an evolutionary dead-end. However, occasionally hybrids might introduce useful genetic material that can help populations adapt to changing conditions. This source of novelty might be more effective than having to wait for a mutation to occur in order to yield a similar result. In the case of butterflies, the effects can be clearly seen on their wings.

Dr Kanchon Dasmahapatra, who worked with Professor James Mallet at University College London added, “What we show is that one butterfly species can gain its protective colour pattern genes ready-made from a different species by hybridizing (or interbreeding) with it. A much faster process than having to evolve one’s colour patterns from scratch.”

The butterfly genus Heliconius is found in the tropical and sub-tropical regions of the Americas, from the Amazon basin to Texas and has been studied by scientists since the Victorian era.

Dr Jiggins added: “The genus Heliconius has been the subject of evolutionary studies since Darwin’s time, and the original formulation of mimicry theory. We are especially interested in them because their convergent wing patterns offer an opportunity to study the repeatability of evolutionary change.”

The sequencing of a butterfly genome also offers some remarkable insights into the biology of these charismatic insects. Butterflies are thought to be more visual in their communication as compared to night-flying moths. Surprisingly, analysis carried out at the University of California by Adriana Briscoe showed that they have an even greater array of genes involved in chemical communication as compared to moths.

Owen McMillan of the Smithsonian Tropical Research Institute in Panama said: “We are accustomed to thinking of butterflies as brightly coloured, primarily visual insects, but the presence of such a rich array of olfactory receptors and chemosensory genes, suggests that smell and taste are also vital.”

The study heralds a new era in genome biology, in which genome sequencing has become available to small groups of researchers for their own organism of choice. In this case academics from 9 labs across the globe each contributed to a pool of funding that permitted the sequencing effort, without any major grant funding.

Dr Jiggins added, “I think it’s been a great privilege to work with all these people across the world, and especially our collaborators in Latin America, who are all equally excited about these butterflies.”

The red eye gene

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I have been meaning to post about another big Heliconius paper that came out earlier this year which made a major advance in our knowledge of the genes underlying Heliconius wing patterning. We have known for some time now, from work led by Simon Baxter in my lab, that a narrow genomic interval is responsible for controlling red wing patterns in both the co-mimics H. melpomene and H. erato. In a paper earlier this year, Bob Reed’s lab made a major advance on this by showing that the optix gene is expressed in a pattern completely correlated with red wing patterns in the developing pupa. This was first uncovered by Riccardo Papa using a microarray experiment, and then elegantly confirmed by Arnaud Martin with in situ hybridisation. Optix is a transcription factor, a gene that regulates the expression of other genes. There are no coding differences between optix sequences in different populations, which shows that regulatory changes underlie the difference in expression.

Here are some links that give more details:
Science perspective article by Sean Carroll
Link to original article

The complexities of a supergene

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A paper describing how Heliconius numata maintains multiple morphs in a single population will be published in Nature on 8 September. This represents many years of work by Mathieu Joron and many others, and shows how genome rearrangements can play a role in adaptation – its a neat story. Here follows part of a press release that went with the paper, and see also a rather neat video produced by Nature:

The study focused on the Amazonian species Heliconius numata, which mimics several other butterfly species at a single site in the rainforest. One population of Heliconius numata can therefore feature many distinct wing colour patterns resembling those of other butterflies, such as the Monarch’s relatives Melinaea, which are unpalatable to birds. This acts as a disguise, protecting them against predators.

The researchers located and sequenced the chromosomal region responsible for the wing patterns in H. numata. The butterfly’s wing-pattern variation is controlled by a single region on a single chromosome, containing several genes which control the different elements of the pattern. Known as a ‘supergene’, this clustering allows genetic combinations that are favoured for their mimetic resemblance to be maintained, while preventing combinations that produce non-mimetic patterns from arising. Supergenes are responsible for a wide range of what we see in nature: from the shape of primrose flowers to the colour and pattern of snail shells.

The researchers found that three versions of the same chromosome coexist in this species, each version controlling distinct wing-pattern forms. This has resulted in butterflies that look completely different from one another, despite having the same DNA.

“We were blown away by what we found”, said Dr Mathieu Joron of the Muséum National d’Histoire Naturelle, who led the research. “These butterflies are the ‘transformers’ of the insect world. But instead of being able to turn from a car into a robot with the flick of switch, a single genetic switch allows these insects to morph into several different mimetic forms – it is amazing and the stuff of science fiction. Now we are starting to understand how this switch can have such a pervasive effect”

Professor Richard ffrench-Constant of the University of Exeter added: “This phenomenon has puzzled scientists for centuries – including Darwin himself. Indeed, it was the original observations of mimicry that helped frame the concept of natural selection. Now that we have the right tools we are able to understand the reason for this amazing transformation: by changing just one gene, the butterfly is able to fool its predators by mimicking a range of different butterflies that taste bad.”
This single supergene also appears important in melanism in other species, including moths. In April 2011, a team led by Liverpool University explained in the journal Science how the Peppered Moth developed its black wings in nineteenth-century Britain’s sooty industrial environment.
“This supergene region not only allows insects to mimic each other, as in Heliconius, but also to mimic the soot blackened background of the industrial revolution – it’s a gene that really packs an evolutionary punch,” added Professor Richard ffrench-Constant.

Butterflies on the prairies

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One of my favourite conferences is always the international biology of butterflies meeting – the general enthusiasm of butterfly people always makes it a stimulating event, and as it only happens every four years or so, there is plenty of time to recover for the next one. The most recent, and now the 6th time the congress has been held, was in Edmonton, Canada last week.

Evolving wings
The Edmonton meeting was no exception to the rule, and there was a generous helping of Heliconius biology to boot. Much of this revolved around wing pattern genetics, with ongoing efforts to identify the genes that control wing patterns finally starting to come to fruition after some ten years of effort in labs on several continents. Perhaps most exciting, the identification of striking expression patterns at a transcription factor previously associated with eye development, by Arnaud Martin and Riccardo Papa, appear to signal the identification of the loci controlling red pattern elements in both Heliconius erato and melpomene. Similarly, Marcus Kronforst has now identified a regulatory gene (transcription factor) that controls the switch between yellow and white in the Heliconius cydno group, while Nicola Nadeau presented data for a cell cycle regulator that is prime candidate for the switching of yellow patterns in Heliconius melpomene.

For me, the identification of these genes has been something of an obsession over the past few years and it is a relief that we are finally close to an answer. The results seem to confirm the hunch that we have had for a while now, that the same genes are involved in producing similar patterns across many Heliconius species. There really is a common ‘toolkit’ of wing patterning genes that are shared across many species. What is surprising is that the genes identified so far do not seem to obviously fall into a single signalling pathway, or interacting network. The challenge now is to figure out how they have evolved to produce the remarkable patterns of Heliconius from their fritillary ancestors, and whether there is something specific to the way patterns are generated that allows such remarkable diversity to be produced in Heliconius.

There was another surprising result presented at the meeting, from linkage mapping projects in Bicyclus (a satyrid or brown butterfly) and the peppered moth. In both species, genes affecting wing patterns (eyespots and melanic wing colouration respectively) map to the same regions of the genome as one of the Heliconius wing patterning genes that was first mapped in our lab. If it really turns out that the same genes are involved in these species, this would imply that there is a shared mechanism for wing evolution across moths and butterflies, which dates back to the time of the dinosaurs. Now that is pretty cool.

Hissing peacocks and new dimensions to communication
One of the most surprising talks for me was a tale of hissing peacocks and mice. Peacock butterflies are known for the stunning eyespots on their wings, which are used to startle predators when they are approached. What is less well known, is that they also make a hissing sound with their wings. This proves remarkably effective at deterring mice, that would otherwise make a meal of them during hibernation. Videos of hibernating butterflies presented by Martin Olofsson showed mice approaching sleeping butterflies, and being startled off by wing flaps, in the complete darkness of a winter roost. It seems that the startle display of the stunning peacock eyespots is complemented by an equally scary audible signal generating by rubbing the wings together. Heliconius cydno are also supposed to make clicking noises (although I have never heard them myself) – perhaps they serve a similar function.

While sounds may be important for some butterflies, a far more ubiquitous mode of communication is through scents. However this remains a black box of butterfly biology, which is only just beginning to be opened. Fritz Muller (famous for the discovery of Mullerian mimicry), was the first to described the feathery ‘androconial’ scales on butterfly wings that diffuse their scents, in the 1860s. In Edmonton, Carla Penz and Naomi Pierce, discussing owl butterflies and blues respectively, both described remarkable patterns of diversity in the placement, shape and form of these androconial patches on the wings. Such rapid evolution generally signals strong selection, and in this case it is likely driven by sexual selection. This was confirmed by Caroline Nieberding, who has identified the compounds that the African butterfly, Bicyclus anynana, uses for sex. The females of this species choose to mate with males based in part on their chemical bouquet, with the older males having a distinct smell that is preferred by females. This makes sense, as older males have survived the trials of life on the African savannah and are therefore more likely to have successful combinations of genes that will produce fit caterpillars. However, the puzzle is why males don’t cheat the system and pretend to be older than they really are by producing the characteristic chemical signal. Perhaps the signals are expensive or difficult to produce, but there is clearly potential for conflict between the sexes in the use of these chemical signals that could lead to an evolutionary arms race and perhaps explain the rapid evolution of the androconial patches and their chemical bouquet.

In Heliconius, a poster by Catalina Estrada described a different set of chemicals known as anti-aphrodisiac pheromones. These have the opposite effect to the Bicyclus sex phermones, and as their name suggests deter mating by males. The chemicals are transferred from males to females at mating, and presumably serve the interests of females who benefit by avoiding pestering by ardent suitors (although such a benefit has yet to be demonstrated). Strikingly there is also a similar pattern of rapid evolution in these chemicals, with closely related species commonly differing in their chemical composition. Catalina has demonstrated that species in the pupal-mating clade evolve more slowly than the non-pupal-maters. This also fits with the idea that conflict could lead to rapid evolution, as among pupal-maters the males call the shots and there is little opportunity for females to choose their partners, while in non-pupal-maters both species can choose so there is more chance for them to differ in opinion – hence more conflict. Once again, sexual conflict is associated with faster evolution of chemical signals.

Researchers are just beginning to explore the world of butterfly scents, and this is clearly an exciting area for future research. No doubt ‘Biology of Butterflies’ in 2014 will have more on this topic…

And more…
Overall the meeting included many more aspects of butterfly biology than I can even begin to mention here. Butterflies continue to be at the forefront of our understanding of the biological response to climate change, with striking range changes very evident at both the warm and cold fringes of species ranges. However, at this meeting there was a shift in emphasis away from simply documenting range changes in response to climate, towards investigating how we might best respond to such changes. Other talks covered so many aspects of butterfly ecology, population biology and evolution that I was exhausted by the end of the week. To recover, we headed south to the Alberta prairies and Drumheller, for some dinosaur therapy.

The genome is on its way – Second HGC meeting

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The Second meeting of the Heliconius Genome Consortium from March 25-26th 2010 was an awe inspiring event, from the decadence of St. John’s College to the impressive data on candidate color pattern genes. However, the focus of the meeting was the Heliconius genome, and with data rolling in from all over, there was plenty to discuss. Chris Jiggins and St John’s College were fantastic hosts, and provided everything we needed to stay caffeinated and involved throughout the days.

Over the two days, Heliconius biologists, bioinformaticians, others from sequencing centers and places of the sort, developed a timeline and framework for annotating, curating, sharing and analyzing the H. melpomene genome. The first freeze and release of an assembled H. melpomene genome could be within the next 3 months. Servers at UCI are already in place in order to hold the sequence data, a BLAST server and a GBROWSE server. Over the coming months CHADO databases will be built, annotation pipelines will be laid, and preliminary genomic analyses will begin.

Beyond the first H. melpomene reference genome being done with 454, we have had our eyes on other races and species of Heliconius to sequence. Plans were outlined for re-sequencing the genomes H. cydno, H. numata, H. erato and more H. melpomene races using Illumina. Plans were also made for RAD-tagging, using Illumina. Mapping families are currently being raised in Panama to create a RAD-tag linkage map for the H. meplomene genome. We are also considering using RAD-tags to scan for population differentiation between the various races of H. erato and H. melpomene. At this point the genome project seemed to be expanding significantly, but the biology was getting a lot more interesting. We just need to convince some funding agencies.

The meeting slowed to a discussion of funds, and how to afford all these awesome experiments. Grant opportunities were discussed and working groups on various topics/aspects relevant to the genome project, were assembled. The meeting ended with a fantastic dinner at the St. John’s College, where they offered many of us way too much wine and port.

All in all, the HGC seems to have a solid game plan, a strong group of interested researchers, some money, and data pouring in, making it very soon that we can expect to see good working draft of the Heliconius genome.