Author Archives: eratosignis

Michel Cast sent me pictures of this nice hybrid specimen from Ceara, Brazil! Thank you Michel and P. Jauffret!

Jacques Mallet[1] @eratosignis

Colour patterns in Lepidoptera evolved mainly as signals to predators. Heliconius are indeed Müllerian mimics. Reply to Mouy (2022).

Abstract

A recent paper in the journal Evolutionary Ecology by Henri Mouy, an independent researcher and theoretician who gives his address as “City of Westminster, London, UK,” argues that aposematism (warning colour) and Müllerian mimicry are problematic hypotheses. Instead, he claims that the bright colours and apparent colour pattern mimicry act primarily as an intraspecific or interspecific communication device to enable aggregation. In this critique, I show that the long-standing understanding that aposematic and mimetic colour patterns communicate directly with predators is much more likely than Mouy’s aggregation hypothesis.

Figure 1. Heliconius erato (above), and H. melpomene (below), a pair of Müllerian co-mimics from different sites in Ecuador and Northern Peru. Each species gains protection from the other’s unpalatability. Within any site, the two species are excellent co-mimics, but major geographic differences in colour pattern have evolved within each species. This geographic diversity is extraordinary by temperate zone standards: the region (about 600km x 300km) of the Andean foothills from which all these forms within each species can be found is less extensive than New England or Great Britain.

Introduction

As a tropical field biologist and geneticist who specializes on the evolution and genomics of Heliconius butterflies (Fig. 1), I try to keep up with the literature. This is becoming an increasingly difficult task, with at least ~50 Heliconius publications per year. While engaged in this activity, I came across a paper by one Henri Mouy titled “Colours as aggregation signals in Lepidoptera: Are Heliconius Müllerian mimics?” The answer to the question in the title, is an emphatic “no!” according to the author. To my surprise, Mouy claims to unseat Heliconius as an example both of aposematic (i.e. warning) coloration, and of Müllerian mimicry (Mouy, 2022), ideas that have been held by evolutionary biologists since their proposals by Bates and Wallace 160 years ago. I therefore read further.

Briefly, Mouy carries out a cursory citizen science analysis of some blurry photos on a British butterfly amateur website. The data, according to Mouy, show that brightly coloured butterflies aggregate more than cryptic or “semi-cryptic” butterflies (Mouy, 2022: his Fig. 1). These data apparently suggest to the author the idea that bright coloration in butterflies (or perhaps all Lepidoptera) evolved “purely as an aggregation signal.”

Then Mouy constructs a mathematical model that purports to show how bright colours can evolve to cause intraspecific attraction to aggregations, where the benefit of the aggregation can outweigh the cost in terms of increased conspicuousness to predators.

Having by now convinced himself that bright coloration in butterflies evolved as an intraspecific signal to enhance aggregation (or maybe in Lepidoptera in general), rather than primarily as a signal to predators, for example, aposematism, including as advertisement for escape ability (Mallet & Singer, 1987), Mouy then moves on to suggest that the reason for close similarity among brightly coloured Heliconius species, usually assumed to be due to Müllerian mimicry, may be incorrect. In support of his aggregation signalling hypothesis for mimetic coloration, he cites my own paper on nocturnal gregarious roosting and mimicry rings in Costa Rican Heliconius (Mallet & Gilbert, 1995), as well as more recent papers on gregarious roosting in Heliconius by Susan Finkbeiner and others (Finkbeiner et al., 2012, Finkbeiner et al., 2014, Salcedo, 2011).

Finally, in sections labelled “Discussion on Heliconius” and “Discussion”, the author strengthens his opposition to accepted theories of aposematism and Müllerian mimicry. In particular, the divergence of mimicry colour patterns between different regions, even within the same species, somehow suggests to the author that aggregation signalling rather than Müllerian mimicry is the cause of colour pattern convergence. The author goes on to argue, without any evidence I could find in his paper, that resemblance by the viceroy butterfly (Limenitis archippus) to monarchs (Danaus plexippus) and queens (Danaus gilippus) evolved “to attract them” (i.e. to attract monarchs, queens and viceroys together). As it happens, I have published a more mainstream view of viceroy mimicry (Mallet, 2001). In the final two sentences of his paper, Mouy argues that the well-known mimicry among unpalatable lycid beetles (Bocak & Yagi, 2010) “may need a reconstruction as well.”

The hypothesis that, to Mouy, explains almost all bright coloration in Lepidoptera and other insects, and also the apparent mimicry between species of Heliconius and other butterflies and beetles is as follows: instead of bright coloration advertising unpalatability to predators, it is an adaptation that advertises aggregations to conspecifics, and these aggregations reduce predation. In my critique below, I attempt to follow Mouy’s logic and sequence of sections.

Association of bright colour with gregariousness, according to Mouy

Mouy’s data extracted from online photographs when plotted against a gregariousness dimension (his Fig. 1) reveal several things. I have cursorily reviewed some of the photos on the cited amateur website.

Firstly, most of these photographs from an British amateur website of butterflies show bright or “semi-bright” coloration. This is hardly surprising, as even British butterflies are relatively conspicuous, and bright colours make butterflies a popular subject for amateur photographers.

Secondly, the majority of photographs show single butterflies, with only a few showing groups of individuals of the same species. Some photos, for instance of monarch butterflies (Danaus plexippus), which are well known to roost in winter aggregations in California and Mexico, do show genuine aggregations. However, for the majority of their life cycle, and indeed during their reproductive cycle, monarchs are notably solitary. Furthermore, there are no images of co-mimics Danaus gilippus and Limenitis archippus aggregating with D. plexippus; heterospecific aggregation is as far as I know unknown behaviour for these latter two species. Other photos, such as a photo with a number of Painted Lady butterflies (Vanessa cardui), clearly shows a large group feeding on a stand of garden nectar plants, presumably due to resource patchiness in a suburban environment rather than to any inherent tendency of this butterfly to aggregate. Mouy discusses similar aggregations also with respect to mud puddling in many butterfly species.

Thus the photos do include a few genuine aggregations, but also some that are clearly examples of concentration due to resource patchiness (such as nectar, or puddling sites). If there is a minor tendency for brighter coloured species to aggregate, there is nothing in these data that indicates colour signalling as the cause of aggregation.

Mathematical model: conspicuous intraspecific signalling supposedly evolves to enhance aggregation

The model proposed by Mouy “determines under which conditions signalling for aggregation through an increase in conspicuousness results in a net reduction in predation.” The model apparently predicts “a reduction in predation when the increase in conspicuousness to co-aggregators is not matched by a proportional increase in conspicuousness to predators.” To paraphrase the verbal result the author I think is reaching for, an increase in conspicuousness to predators can evolve if the benefit of signalling to conspecifics to form an aggregation (which is argued to reduce predation) outweighs the increased cost due to conspicuousness to the predators (which could increase predation). However, it is most unclear whether this actually models the aggregation signalling hypothesis.

The author argues rather vaguely for a “dilution effect” of aggregation. However, while a kind of dilution effect is involved in all hypotheses of aposematism and Müllerian mimicry, as well as of aggregation under conditions of predation, this requires modeling frequency-dependent or “number-dependent” selection (Mallet & Joron, 1999), both of which are conspicuously absent from the authors’ mathematical model. The current model subsumes the whole of this frequency-dependent complexity into a constant parameter, D_pred , “the increase in the probability of detection to predators.” The results are then displayed in a graph of change in overall “predation risk” (Mouy 2022: his Fig. 2), although how time is factored into predation risk is not discussed in the main paper. The author argues that “predation is reduced as a result of signalling when the result is below zero.” The axes are unlabeled, and it is not quite clear what “the result” is, although the reader infers that the x axis refers to time, and the y axis to “the result”, which varies from -20% to +20%; this presumably means some measure of predation risk. I would have thought that a 0% predation risk would be optimal, but according to the author a negative risk percentage is even better, though it is somewhat unclear what a negative predation risk would be.

In the modelling section of the main paper the author refers repeatedly to details in online Appendices 4, 5 and 6. In those appendices I found various scantily documented mathematical formulae, more graphs with unlabeled axes, some python code, and extensive tables of results. However, there was very little in the way of clear explanation. I was able to take away the idea that the author somehow models prey numbers or density by means of encounter rate over time, but not really how the “dilution effect” is supposed to work or what the benefit of aggregation was supposed to be. The mathematical model presented here is not a recognizable model of populations or their evolution over time.

Heliconius: shared aggregation signal or Müllerian mimicry?

This section, as well as Mouy’s following section (Discussion on Heliconius), and the final discussion are the main parts of the paper (Mouy, 2022) that deal with aposematism (warning colour) and mimicry. He classifies aposematism somewhat obscurely as “a visible structure which alters predators [sic] behaviours, which evolved or failed to disappear because of that effect and which is effective because predators either evolved or learned a response to that signal.” However, in his online Appendix 2, it becomes clear that the author does understand that aposematism is a theory of warning signals that communicate to the predator some sort of prey unprofitability. Apparently the author regards the theory of aposematism unlikely: “As reviewed in online appendix 2, the maintenance of an aposematic signal requires either peak-shift on the part of predators (or another indistinguishable mechanism), or kin-selection (Leimar et al., 1986), or potentially some other enabling mechanism such as innate aversion or neophobia. None are observed in Heliconius.” Mouy gives no evidence for this latter statement. In fact, the maintenance of aposematism has never been seen as a problem by most other authors since Wallace (1867); it acts as a mutualism between predator and prey that avoids damage to either, and is particularly advantageous to the prey. The maintenance of aposematism once established is easy to understand because all individuals in a local prey population benefit from the shared signal to warn the mostly educated predators in a community away.

It is the origin of aposematism that is sometimes seen as problematic: it might involve “peak shift,” “kin selection” or “some other enabling mechanism.” Rare conspicuous individuals among majority less conspicuous individuals could suffer greater initial predation costs because the predators perhaps do not recognize the new signal of an unprofitable species. Nonetheless, I personally believe that warning colours often, and perhaps mostly evolved via individual selection. The various routes that seem likely are colour pattern enhancement (including behavioural “peak shift”), receiver bias, and of course mimicry (Mallet & Singer, 1987, Mallet & Joron, 1999, Ruxton et al., 2018). Alternative explanations could involve a generalization of the population structure model “kin selection,” “kin-founding” or “shifting balance” models, but these are more controversial (Mallet, 2010).

Apart from his dismissive statement that “Heliconius are not even particularly colourful by butterfly standards,” I cannot find any other cited evidence why Mouy might reject the prevailing and well-accepted idea that Heliconius are aposematic. Heliconius colour patterns include crimson bands, matte black, yellow bars, orange rays, stripey contrasts, and sometimes iridescent blue which flashes in the sunlight (Fig. 1). In contrast to Mouy, I guess most people who have seen Heliconius would agree that they are among the most brightly coloured butterflies!

Müllerian mimicry

So much for aposematism. But Heliconius are classically viewed also as Müllerian mimics. In fact, Müllerian mimicry was a major component of Bates’ (1862) original hypothesis of mimicry, especially between Heliconius and ithomiine butterflies, and among different species of Heliconius. Bates argued that rare Heliconius mimicked commoner species of ithomiines (which he called “Danaoid Heliconidae.” A little later, a German émigré in Brazil, Fritz Müller proposed almost certainly the first mathematical model of Darwinian fitness under natural selection (Müller, 1879) in his argument for what is now termed Müllerian mimicry. He could have applied the hypothesis to local Brazilian species of Heliconius, but he focused on a different pair of species of Danaini and Ithomiini. Today, Heliconius is widely used in examples of Müllerian mimicry (Mallet & Joron, 1999, Mallet, 2001, Futuyma & Kirkpatrick, 2017, Ruxton et al., 2018).

Of course, a venerable one hundred and sixty-year old tradition of study of a topic does not necessarily mean that the prevailing view is correct, but it ought at least make the author of any alternative hypothesis take some care when attempting to disprove previous work. Yet very little effort seems to have been expended by Mouy (2022) to rebut the perceived consensus.

Mouy’s aggregation signalling hypothesis

Mouy’s alternative to aposematism and Müllerian mimicry is his own “aggregation signalling hypothesis”. According to Mouy, classical understanding of signalling to predators fails. Instead, conspicuous colours and close mimicry among species enables signalling within and between species of prey in order to aggregate. Aggregation is beneficial because of a dilution effect that reduces per capita predation.

The more probable explanation of aggregations is a reverse of this logic. In an aggregation of a particular size, unprofitable prey will suffer lower per capita mortality than an aggregation of more profitable prey because predators are satiated by fewer unpalatable than palatable individuals. Therefore, if predation is likely, we expect unprofitable prey (including aposematic prey) to be more prone to aggregate than profitable prey. Aggregation can also benefit even palatable individuals via satiation. This is also an old idea: one of the most famous proponents was the “selfish herd” hypothesis of Bill Hamilton (Hamilton, 1971), but it is older than that. Poulton spent many years collating examples of gregariousness in aposematic butterflies (Poulton, 1890, Jones, 1930, Poulton, 1931c, Poulton, 1931a, Poulton, 1931b, Poulton, 1933).

How could the extraordinarily accurate “mimicry” among Heliconius species evolve? Mouy (2022) argues not only that conspicuous colour patterns are examples of adaptations that originated as aggregation signals within species, but also that the tight similarity (mimicry) among species is favoured in signalling to attract other species to their aggregations. Here Mouy cites my own work on gregarious roosting in a community of Heliconius (Mallet & Gilbert, 1995) in support of aggregation signalling (Mouy, 2022): we found heterospecific aggregations of Heliconius species that preferentially (although not only) involved co-mimics, and we did conclude that “it therefore seems likely that individuals actively select co-mimics as roost-mates.”

However, it is most unlikely that aposematism and mimicry is primarily an aggregation signal, for a variety of reasons:

1) As Mouy admits, “birds have a much better visual acuity than butterflies … Modelling how a butterfly … would be seen by conspecifics and predators, it is found that the complex patterns are usually not resolvable by conspecifics, but that the whole-body coloration are still resolvable, and thus can function as an intraspecific signal. Predators have a considerably better acuity, can resolve the shape of butterflies at a distance and are likely attracted to butterfly wing shapes.” This view of insect vision is generally accepted, and argues against Mouy’s aggregation signalling hypothesis. Insects have excellent colour vision, motion detection and contrast perception. But insect vision is highly pixellated, and insects do not have good shape perception, compared with vertebrate vision. Yet mimicry among Heliconius species is so accurate that even experts are sometimes fooled, and fail to distinguish the species — almost all major butterfly collections in the world museums I have visited have some misidentifications for this reason. The highly accurate shape perception that we vertebrates use to detect the clear cases of Heliconius mimicry is a communication channel unavailable to insects. A mere convergence in “whole body coloration” would not require detailed resemblance in shape of pattern outlines.

2) Mouy ignores a section in our paper where we discuss how mimicry colour patterns are often involved as intraspecific cues in mate choice, and their association with speciation (Mallet & Gilbert, 1995: 176). Heliconius cydno (including its semispecies allies, H. pachinus and H. timareta) differs from its sibling species H. melpomene. The latter is red and black with a yellow hindwing bar, and males in particular tend to be attracted to red rags waved in the forest; H. cydno, on the other hand is white and black often with iridescent blue in the melanic regions, and is attracted instead to white rags. Notice that these signals are non-specific as the coloured rags do not look much like real Heliconius butterflies. We concluded that “while mate choice may evolve during mimetic divergence, it is rather unlikely that evolution of mate choice itself drives divergence” (Mallet & Gilbert, 1995: 176).

We later showed experimentally that colour is indeed involved in the initial courtship approach by males of these two species to females, or to crude coloured paper models (Jiggins et al., 2001). We thought that perhaps most speciation in Heliconius was accompanied by a mimicry switch (Turner, 1976). But colour pattern loci acting as important “speciation genes” is not the norm even in Heliconius. We later discovered that highly mimetic forms of H. timareta (part of the H. cydno superspecies) were sympatric with identically patterned H. melpomene (Giraldo et al., 2008, Mérot et al., 2013). Later genomic work proved that H. timareta gained its colour pattern mimicry via occasional hybridization with the local forms of H. melpomene (Heliconius Genome Consortium, 2012). These cryptic pairs of sympatric forms were previously confused by workers on Heliconius, including myself. Similarly, we recently discovered another cryptic pair of sister species in a different subgroup of Heliconius, H. eratosignis and H. demeter, that also share mimetic patterns, and yet successfully remain distinct in sympatry (Rosser et al., 2019). Thus although intraspecific preferences do sometimes make use of differences in mimetic colour patterns, they are not the primary feature keeping species apart. Instead, pheromone differences between species are almost certainly the most important cue that leads to strong assortative mating among these species (Mérot et al., 2015, Jiggins et al., 2001). Similarly, it is most unlikely that aggregation signalling is the primary function of mimetic colour patterns.

3) As it happens, a certain amount is known about cues that attract Heliconius to gregarious roost mates, and it conflicts with Mouy’s aggregation signalling hypothesis for mimicry and bright colour patterns. As with courtship, roosting aggregation involves an initial generalized approach to a visual cue, followed by a close range “fanning” or hovering behaviour, during which time both males and females appear to exchange odour cues (Mallet, 1980, Mallet, 1986). It is likely, in fact, that courtship behaviour has been coopted in these species to facilitate aggregation behaviour. While colour pattern and contrast patterns are involved in initial attraction, even crude black or white oblong cardboard models can elicit close approach and fanning behaviour if in a setting that is contrasty enough (Mallet, 1980). Furthermore, there are plenty of examples of non-mimics roosting gregariously, in spite of a bias towards co-mimics (Mallet & Gilbert, 1995). Detailed mimicry is clearly not required for attraction of Heliconius to heterospecific roosts.

Is the theory of aposematism and mimicry in need of a revision? (The answer is no!)

In science, no hypothesis is actually proved. Rather, we tend to disprove alternatives, or at least to show why the alternative hypotheses are unlikely. Sometimes, however, prevailing opinion is overturned. For instance, before Copernicus, people generally seem to have believed the Ptolemaic theory that the sun revolved around the earth. The Copernican/Newtonian revolution explained that it was more likely instead that the earth revolved around the sun, with the mechanism for elliptical orbits being gravity. Today no serious scientist believes any alternative, and alternatives now seem so unlikely that one can say that rotation round the sun is an established fact. So is Henri Mouy a new Copernicus of mimicry theory? Or is his aggregation hypothesis just wrong? It seems clear that the latter is the correct interpretation.

One hundred and sixty years ago, the evolutionary hypothesis of mimicry was born (Bates, 1862): predators avoid attacking prey that are unprofitable and learn to recognize their colour patterns and avoid them; other either palatable or unpalatable species benefit from reduced predation pressure by having copy-cat  colour patterns. Soon after, the hypothesis of warning colour was proposed to explain bright colour patterns in unpalatable insects (Wallace, 1867): individuals displaying these advertising colour patterns were recognized by predators, after conditioning by previous encounters, and avoided as prey. This evolutionary theory of warning coloration as a signal was conceptualized as “aposematism” by a classically educated Oxford University entomologist who enjoyed coining neologisms based on Greek roots (Poulton, 1890) – “sympatry” was another term he coined. Although there are some who would question minor details of mimicry and warning coloration, almost all of today’s work on the phenomena of mimicry and aposematism accepts these ideas as being largely correct. The bright aposematic colour patterns of skunks and wasps are so clearly warnings that nobody doubts it; the examples of wasp mimicry by flies and Lepidoptera have nothing to do with aggregations, and show that these signals are indeed learnt by potential predators, just as humans learn to avoid wasps after being stung. These same hypotheses are supported in most evolution textbooks (Futuyma & Kirkpatrick, 2017, Ruxton et al., 2018). A rejection of these ideas would be a major upset in evolutionary biology.

Evolutionary theories of aposematism and mimicry were initially based on comparative evidence and theory. These ideas were later backed up with extensive observations of the behaviour of birds and their interactions with insects; Poulton was especially active in the early part of the 20^th Century in gathering and publishing observations from around the world (see above). In 1958 the first carefully controlled behavioural experiments on mimicry were carried out (Brower, 1958), and soon thereafter with heliconiine butterflies (Brower et al., 1963). Subsequently experiments in field and laboratory have carefully documented predator perception and learning, prey behaviour, and the strength of natural selection, as well as other evidence on the function of aposematism, mimicry and aggregations of potential prey on predators (Mallet & Joron, 1999, Jiggins, 2017, Ruxton et al., 2018). Heliconius remains an extraordinarily useful model genus for understanding the evolution of mimicry and aposematism, and there really is no doubt that that aposematism and mimicry are very strongly supported as the primary explanation for bright colours. In contrast, although colour patterns are sometimes exploited in a general way by Heliconius as intraspecific cues, this is clearly only a secondary re-use rather than the primary function for the bright colours and mimicry.

Conclusion

I am somewhat astonished that Henri Mouy, an “independent researcher,” who provides no observations of his own on butterflies in the wild, seems to have persuaded the editors and reviewers of an academic journal that his hypothesis might overturn consensus, a century and a half old, on warning colour and Müllerian mimicry.

Acknowledgments

I am very grateful to Graeme Ruxton, an Editor at Evolutionary Ecology, for considering this piece for publication in Evolutionary Ecology as a rebuttal. However, I decided that it would be better as a blog post. I am also grateful to Henri Mouy for his correspondence on the issue, and to my lab group (Neil Rosser, Fernando Seixas, Yuttapong Thawornwattana, and Sarah Dendy) for advice.

References

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Bocak, L. & Yagi, T. 2010. Evolution of mimicry patterns in Metriorrhynchus (Coleoptera: Lycidae): the history of dispersal and speciation in south east Asia. Evolution 64: 39-52.

Brower, J. V. Z. 1958. Experimental studies of mimicry in some North American butterflies. Part I. The monarch, Danaus plexippus, and viceroy, Limenitis archippus archippus. Evolution 12: 32-47.

Brower, L. P., Brower, J. V. Z. & Collins, C. T. 1963. Experimental studies of mimicry. 7. Relative palatability and Müllerian mimicry among Neotropical butterflies of the subfamily Heliconiinae. Zoologica, New York 48: 65-84.

Finkbeiner, S. D., Briscoe, A. D. & Reed, R. D. 2012. The benefit of being a social butterfly: communal roosting deters predation. Proceedings of the Royal Society B: Biological Sciences 279: 2769-2776.

Finkbeiner, S. D., Briscoe, A. D. & Reed, R. D. 2014. Warning signals are seductive: relative contributions of color and pattern to predator avoidance and mate attraction in Heliconius butterflies. Evolution 68: 3410-3420.

Futuyma, D. & Kirkpatrick, M. 2017. Evolution. Fourth Edition.Sinauer, Sunderland, Mass.

Giraldo, N., Salazar, C., Jiggins, C. D., Bermingham, E. & Linares, M. 2008. Two sisters in the same dress: Heliconius cryptic species. BMC Evolutionary Biology 8: 324.

Hamilton, W. D. 1971. Geometry for the selfish herd. Journal of Theoretical Biology 31: 295-311.

Heliconius Genome Consortium 2012. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature (London) 487: 94-98.

Jiggins, C. D. 2017. The Ecology and Evolution of Heliconius Butterflies.Oxford University Press, Oxford.

Jiggins, C. D., Naisbit, R. E., Coe, R. L. & Mallet, J. 2001. Reproductive isolation caused by colour pattern mimicry. Nature (London) 411: 302-305.

Jones, F. M. 1930. The sleeping heliconias of Florida. Natural History 30: 635-644.

Leimar, O., Enquist, M. & Sillén-Tullberg, B. 1986. Evolutionary stability of aposematic coloration and prey unprofitability: a theoretical analysis. American Naturalist 128: 469-490.

Mallet, J. 1980. A laboratory study of roosting in the gregarious butterfly Heliconius melpomene. UCL Discovery.

Mallet, J. 1986. Gregarious roosting and home range in Heliconius butterflies. National Geographic Research 2: 198-215.

Mallet, J. 2001. Causes and consequences of a lack of coevolution in Müllerian mimicry. Evolutionary Ecology 13: 777-806.

Mallet, J. 2010. Shift happens! Evolution of diversity in warning colour and mimicry. Ecological Entomology 35: 90-104.

Mallet, J. & Gilbert, L. E. 1995. Why are there so many mimicry rings? Correlations between habitat, behaviour and mimicry in Heliconius butterflies. Biological Journal of the Linnean Society 55: 159-180.

Mallet, J. & Joron, M. 1999. The evolution of diversity in warning colour and mimicry: polymorphisms, shifting balance, and speciation. Annual Review of Ecology and Systematics 30: 201-233.

Mallet, J. & Singer, M. C. 1987. Individual selection, kin selection, and the shifting balance in the evolution of warning colours: the evidence from butterflies. Biological Journal of the Linnean Society 32: 337-350.

Mérot, C., Frérot, B., Leppik, E. & Joron, M. 2015. Beyond magic traits: multimodal mating cues in Heliconius butterflies. Evolution 69: 2891-2904.

Mérot, C., Mavárez, J., Evin, A., Dasmahapatra, K. K., Mallet, J., Lamas, G. & Joron, M. 2013. Genetic differentiation without mimicry shift in a pair of hybridizing Heliconius species (Lepidoptera: Nymphalidae). Biological Journal of the Linnean Society 109: 830-847.

Mouy, H. 2022. Colours as aggregation signals in Lepidoptera: Are Heliconius Müllerian mimics? Evolutionary Ecology 36: 341–353.

Müller, F. 1879. Ituna and Thyridia; a remarkable case of mimicry in butterflies. Proceedings of the Entomological Society of London 1879: xx-xxix.

Poulton, E. B. 1890. The Colours of Animals.Trübner & Co Ltd, London.

Poulton, E. B. 1931a. Acraeine butterflies congregating in a small area for the night’s rest, observed by Dr. Hale Carpenter in Portuguese East Africa. Proceedings of the Entomological Society of London 6: 71-.

Poulton, E. B. 1931b. The gregarious sleeping habits of a heliconian and an ithomiine butterfly in Trinidad, observed by P. Lechmere Guppy. Proceedings of the Entomological Society of London 6: 68-69.

Poulton, E. B. 1931c. The gregarious sleeping habits of Heliconius charitonia, L. Proceedings of the Entomological Society of London 6: 4-10.

Poulton, E. B. 1933. The gregarious resting habits of danaine butterflies in Australia; also of heliconiine and ithomiine butterflies in tropical America. Proceedings of the Royal Entomological Society of London 7: 64-67.

Rosser, N., Freitas, A. V. L., Huertas, B., Joron, M., Lamas, G., Mérot, C., Simpson, F., Willmott, K. R., Mallet, J. & Dasmahapatra, K. K. 2019. Cryptic speciation associated with geographic and ecological divergence in two Amazonian Heliconius butterflies. Zoological Journal of the Linnean Society 186: 233-249.

Ruxton, G. D., Allen, W. L., Sherratt, T. N. & Speed, M. 2018. Avoiding Attack: The Evolutionary Ecology of Crypsis, Aposematism, and Mimicry. Second Edition.Oxford University Press, Oxford.

Salcedo, C. 2011. Evidence of predation and disturbance events at Heliconius (Insecta: Lepidoptera: Nymphalidae) nocturnal aggregations in Panama and Costa Rica. Journal of Natural History 45: 1715-1721.

Turner, J. R. G. 1976. Adaptive radiation and convergence in subdivisions of the butterfly genus Heliconius (Lepidoptera: Nymphalidae). Zoological Journal of the Linnean Society 58: 297-308.

Wallace, A. R. 1867. Mimicry and other protective resemblances among animals. Westminster and Foreign Quarterly Review 32: 1-43. [Note added 20 Jan 2024: The warning colour (aposematism) hypothesis is not well developed in this paper. I think the Wallace reference I was thinking of is: Wallace, A.R. 1867. Letter 5416 – Wallace, A. R. to Darwin, C. R., 24 Feb 1867, Reply to Darwin about brightly coloured catterpillars (sic), 8 pp. Darwin Correspondence Project. Cambridge, University of Cambridge. https://www.darwinproject.ac.uk/letter/DCP-LETT-5416.xml.]

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[1] Cambridge, MA, USA

Henri Mouy has recently answered my criticism. See: https://www.heliconius.org/2024/heliconius-are-neither-aposematic-nor-mullerian-mimics-henri-mouy-on-mallet-2024-on-mouy-2022/

A fascinating recent paper by Jennifer Hoyal Cuthill et al. (2019) published in Science Advances uses a “deep convolutional neural network” to classify photos of upper and underside of 1234 butterfly specimens, all of them named subspecies of Heliconius erato and H. melpomene, into phenotypic clusters. The researchers worked with Blanca Huertas and Robyn Crowther to photograph specimens from the London Natural History Museum, that has one of the most complete collections of Heliconius worldwide. They compare the “phylogenetic analyses” based on phenotypic classification with those of genes known or thought to be close to sites of colour pattern switch loci, and those of “neutral” genes selected from around the genome. They conclude that the species have converged within each geographic region, due to Müllerian mimicry. They also argue that the results prove that convergence is due to mutual coevolution.

This topic is of particular interest to me because (a) it concerns my favourite organisms, (b) the coevolution conclusion rebuts a paper I wrote arguing that there is little convincing evidence for coevolution in Müllerian mimicry (Mallet 2001). I’ve communicated with Jennifer on the paper, and discussed the difficulty of classifying hybrids between races, and helped to correct her classifications with some of the obvious inter-subspecific hybrids I found in a sample of their photos from the Natural History Museum’s collections of each subspecies. Blanca Huertas also was my PhD student at UCL, so I am somewhat conflicted about this paper.

Firstly how does the algorithm perform? I don’t fully understand how the deep convolutional neural network works, and in fact maybe nobody really does, but the algorithm itself apparently does! It clearly classifies some mimics together. For instance H. erato phyllis is reasonably near H. melpomene nanna and H. melpomene burchelli in Fig. 1A, which is expected because they are usually classified as co-mimics. I assume that the Euclidean “phenotypic distance” referred to in this figure is measured in 64-dimensional space using the algorithm’s classification of each specimen.  But H. erato venustus (https://butterfliesofamerica.com/L/heliconius_erato_venustus.htm) is classified by the algorithm a long way from its common co-mimic in Bolivia H. melpomene penelope (see: http://media.api.aucklandmuseum.com/id/media/v/576002?rendering=original.jpg for a series of the pure subspecies). For some reason penelope is not called a mimic according to the colour coding in Fig. 1, for reasons I don’t understand. And penelope (no. 28) and four other numbered subspecies are completely missed from Table 1, for reasons that are not explained. I am wondering if the Natural History Museum just happens not to have a good collection of pure penelope, and that’s why we have this apparent screw up. It was mentioned in the methods that there was only one “pure” penelope, and maybe it happened to be one of the obvious hybrids in the type series in the Natural History Museum (https://butterfliesofamerica.com/L/t/Heliconius_melpomene_penelope_a.htm). Also, Heliconius melpomene vulcanus is mis-classified to be phenotypically close to H. m. melpomene and H. erato hydara both of which lack a yellow hindwing bar that vulcanus has on the underside, and penelope which is rayed. The authors say that this is because the blue iridescence of H. melpomene vulcanus is reduced compared to the true comimic from Western Colombia, H. erato venus (p. 3). This is true, although this may also be due to the use of photographs taken in artificial light rather than under natural sunlit conditions. Some Heliconius colours, particularly iridescence, are particularly hard to render photographically.

Table 1 itself also shows that penelope groups fairly closely with H. melpomene burchelli and nanna, but that H. erato phyllis is not classified together with these two, but instead with Heliconius erato petiverana from Mexico. In sum, the algorithm, after being trained on 1500 images, does a reasonably good job of classifying the remaining 968 images to subspecies with 86% accuracy. Interestingly, some of the principal component axes (3 and 4) are apparently also able to distinguish H. erato and H. melpomene (Fig. 2F), suggesting that some useful phylogenetic information, as well as mimicry, is detected by the algorithm.

Overall, I’m reasonably impressed with the algorithm’s performance, although it seems only to reach a not-so good taxonomists’ level thus far: a good human taxonomist will still beat it. Deep Convolutional Neural Network (ButterflyNet) is not yet the Deep Blue of taxonomy! But this is the first time I believe that such an extensive classification of this nature has been done by machine learning, and so this represents a considerable achievement for this paper and these authors.

Next, let’s consider the evidence for the authors’ argument for coevolution in Müllerian mimicry. Readers will probably be aware that Müllerian mimicry occurs between species that are both generally rejected by predators, and it is classified as a mutualism because both partners in the mimicry ring benefit. Mimicry evolves because each species benefits from the association due to mortality during predator learning; each species is sharing the costs of educating predators. On the other hand, Batesian mimicry is the case where an edible species evolves to mimic a poisonous species. In this case, the relation is parasitic, because a pleasant experience with an edible mimic may induce a predator to attack the model. The alternative is one-sided “advergent” mimicry (Brower & Brower 1972), whereby a mimic converges to an unpalatable model, but the model does not respond by evolving towards the mimic. Advergent mimicry is expected in parasitic Batesian mimicry, while Müllerian mimicry is a mutualism, and most people imagine that all mutualisms involve coevolution.

First we need some history. Müllerian mimicry has two special features.

First, Müller’s paper was indeed “evolution’s oldest mathematical model” (Müller 1879). Müller was a maths teacher at the college at Desterro, Brazil as well as a correspondent of Darwin and a major naturalist who documented the local fauna and flora. Müller suggested that predators probably learned to avoid unplatable species after killing a certain number of these per year. If two unpalatable prey species shared the same colour pattern so that they were indistinguishable to the predators, then they would each lose fewer individuals killed during the process of learning, making this a mutualism. We expect the rarer species to gain most of the association. Müller showed that each species gains a proportional advantage by becoming an indistinguishable mimic given by the inverse square of the relative abundance. For example, if a species has a tenth of the abundance of its comimic, it gains 100x the fitness benefit from the mimicry. The same will apply to the degree of unpalatability; measured as the reduction in the number killed, unpalatability and abundance combine to reduce predation in the same way (Mallet 2001). Thus, the benefits of Müllerian mimicry will typically be very one-sided unless abundance and unpalatability are closely balanced.

Second, there’s another wrinkle. John R.G. Turner (1977, 1988), citing a 1927 paper by A.J. Nicholson, pointed out that an abundant unpalatable species would typically not gain by mimicking a rarer unpalatable species, because local predators will be better trained by the most abundant (and/or most unpalatable) species. Therefore, a common or very unpalatable mimic has very little interest in converging on a rarer or less unpalatable species, even though, once it did occur, it would ultimately be beneficial for both species (albeit much reduced by the Müller inverse square law for the common species). Turner argued that most Müllerian mimicry would occur with rarer species approaching commoner species and gaining the evolutionary benefits of mimicry. In his “two-step” model, however, Turner did also propose a subsequent truly coevolutionary mechanism for Müllerian mimicry. Once the proto-mimic species overlapped the model species due to advergence in the first step of mimicry, and became somewhat indistinguishable in the perceptual consideration of the predators, then the second step, mutual convergence, became possible (Turner 1977, 1984, 1988).

Thus these two considerations argue that coevolution will occur perhaps rarely between Müllerian mimics, unless some lucky combination of density fluctuations or palatability details are met, at least until after the two species become so close as to be within a tight domain of protection by the most common species.

What is the evidence for coevolution among Heliconius co-mimics in nature? My own PhD supervisor, Larry Gilbert, had suggested that it was clear that normally, H. melpomene adverged to H. erato, but he argued that some evidence suggested that the reverse could also be true. In Central America, H. melpomene rosina has a broad yellow hindwing band. In contrast, H. erato petiverana from Mexico, and H. erato forms southward to northeastern Costa Rica also have narrow yellow hindwing bands. Heliconius melpomene is a southern species in Central America, and enters Nicaragua but is not known from further north. Gilbert suggested that although the prevailing direction of mimicry was melpomene -> erato, nevertheless in the case of the hindwing bars, the broadening of the yellow hindwing bar to the south of the H. erato distribution is due to convergent mimicry with the broader bands of H. melpomene (Gilbert 1983). I disputed that. Heliconius erato may have diverged in northern populations to produce narrow yellow bars, but since it did not occur there, H. melpomene would not have been able to follow this trend in the north. In contrast, the main mimicry force on H. melpomene in the south would be to adopt the broader hindwing bars of the local H. erato. Thus the apparent spatial coincidence of H. melpomene rosina and H. erato forms with broad yellow hindwing bars is readily explained by mimicry, but not necessarily by means of coevolution and mutual convergence.

In my own paper I concluded that the null hypothesis for coevolution had not been effectively rejected, and that most indications suggested H. melpomene was largely an advergent mimic of H. erato rather than the other way round. This was evidenced by the generally greater abundance, more widespread geographic distribution, and neater colour patterns of the latter – H. melpomene, although often an extremely accurate mimic, tends to have fuzzier or more variable colour patterns and, together with close sister species H. cydno and H. timareta, mimics a variety of other species or subspecies in the Heliconius erato-sara group of species.

In the new paper, Hoyal Cuthill et al. (2019) follow on from previous attempts (Hoyal Cuthill & Charleston 2012, 2015) to prove that coevolution did in fact occur between H. erato and H. melpomene. Some of their arguments are: (1) based on molecular dating, the subspecies of the two species are roughly the same age, as would be expected if they had co-diverged in different geographic localities, (2) that genealogical topologies of colour pattern genes are more similar to those of co-mimics than are genealogies based on a set of comparator genes more distantly linked to colour pattern genes, and (3) arguments similar to those of Gilbert (1983) about divergence of races of H. erato in the absence of H. melpomene. For instance, Hoyal Cuthill et al. (2019) argue that the narrow red forewing band of W. Ecuador H. erato cyrbia (see figure) is an example of advergence towards narrow-banded H. melpomene cythera (rather than the other way round), apparently because the adjacent Colombian H. melpomene vulcanus also displays a somewhat narrower forewing band than H. erato venus in this western part of South America.

However, for (3) most colour pattern features of H. melpomene cythera indicate fuzziness and variability, as expected if melpomene is approximating the tidy and extraordinarily striking pattern of H. e. cyrbia, rather than being mimicked. The already noted dullness of the blue iridescence of melpomene vulcanus compared with erato venus is cranked up to even greater pitch with melpomene cythera versus erato cyrbia. This suggests that H. melpomene evolutionarily attempts to, but finds it so far impossible follow the extreme flashiness of H. erato cyrbia, and here I mean this literally, if you’ve ever seen cyrbia flying in the sunlight.

I’m not convinced by (2) either, since although Hoyal Cuthill et al. picked “colour pattern genes”, these genes were not at the precise location of colour pattern loci, which are known to be largely in gene desert non-coding regions nearby; they mostly appear to be cis-regulatory elements that control the effector genes. Phylogenetic topologies based on these genes are also similar to topologies based on unlinked loci. I remain also unconvinced by (1), in part because it is circumstantial evidence (same age does not equal coevolution), and in part because we don’t really know how to age subspecies via molecular genetic data given the abundant gene flow between subspecies at their hybrid zones (Nadeau et al. 2012).

The discussion ends with a hypothetical model of how some colour pattern traits might recombine across mutualists so that novel traits can evolve in both species as a result of mutual coevolution and convergence. I agree that this would be true if coevolution was the case, but first I’d need to be convinced that coevolution did occur. For instance, a novel trait for Heliconius erato/melpomene mimicry in H. e. cyrbia is the white hindwing fringe checked with black rays, which does not occur in any other race of this species. Heliconius melpomene also has a version of this novel trait in subspecies cythera, but just knowing that does not make it clear which species first invented it or whether it represents a combination due to mutual convergence.

Overall, this is a fascinating and complicated paper. It achieves for the first time a machine learning classification of the mimicry patterns in Heliconius erato and H. melpomene. But I believe it does not yet prove the case for coevolution between these two iconic co-mimics. 

References

Brower, L.P., & Brower, J.V.Z. 1972. Parallelism, convergence, divergence, and the new concept of advergence in the evolution of mimicry. Transactions of the Connecticut Academy of Arts and Sciences 44:57-67

Gilbert, L.E. 1983. Coevolution and mimicry, Pages 263-281 in D.J. Futuyma, ed. Sunderland, Mass., Sinauer Associates

Hoyal Cuthill, J., & Charleston, M. 2012. Phylogenetic codivergence supports coevolution of mimetic Heliconius butterflies. PLoS One 7:e36464

Hoyal Cuthill, J.F., & Charleston, M. 2015. Wing patterning genes and coevolution of Müllerian mimicry in Heliconius butterflies: support from phylogeography, cophylogeny, and divergence times. Evolution 69:3082-3096

Hoyal Cuthill, J.F., Guttenberg, N., Ledger, S., Crowther, R., & Huertas, B. 2019. Deep learning on butterfly phenotypes tests evolution’s oldest mathematical model. Science Advances 5:eaaw4967. https://advances.sciencemag.org/content/advances/5/8/eaaw4967.full.pdf

Mallet, J. 2001. Causes and consequences of a lack of coevolution in Müllerian mimicry. Evolutionary Ecology 13:777-806

Müller, F. 1879. Ituna and Thyridia; a remarkable case of mimicry in butterflies. Proceedings of the Entomological Society of London 1879:xx-xxix

Nadeau, N.J., Whibley, A.C., Jones, R.T., Davey, J.W., Dasmahapatra, K.K., Baxter, S.W., Quail, M.A., ffrench-Constant, R.H., Blaxter, M., Mallet, J., & Jiggins, C. 2012. Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing. Philosophical Transactions of the Royal Society B: Biological Sciences 367:343-353

Kelsey Byers (@plantpollinator) has posted a very useful list of talks and posters at Evolution 2018 Montpellier on Heliconius and related topics such as mimicry and Ithomiini.

See: https://twitter.com/eratosignis/status/1029394638539509760

and:

https://docs.google.com/document/d/1WC8P5ai7k34g24S0XxkZ3pnkZm-DF-WLEKwSJvBUmgI

In front of Museum of Comparative Zoology, Cambridge, Mass.

Blanca Huertas, chief coordinator of the Tropical Andean Butterfly Diversity project (TABD), has just posted the following message on the TABD mailing list http://www.mailinglists.ucl.ac.uk/mailman/listinfo/tabd :

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Dear colleagues,

On 23 May 2011 (7 years ago today), we made an important announcement, that quite rightly predicted that the history of butterfly research will change forever..

With thanks to Professor Dr Gerardo Lamas’ work on butterflies for various decades, the Tropical Andean Butterfly Diversity Project TABD and the Darwin Initiative funding, the Butterflies of America team and every person involved in the process of scanning and digitising Prof Lamas huge collection of photos of types, it was possible to provide free online access to this endless source of knowledge.

Please take a moment to read the original announcement (below) sent six years ago and learn the story behind the Neotropical Types in Butterflies of America.

Please note the TABDP mailing list is still active after 10 years and there for you to register!

It is definitively a moment to remember, to celebrate, to assess how much things have changed since and why not, to contribute and make BOA better with your photos and contributions.

All the best y un saludo!

Blanca

Blanca Huertas PhD FLS DIC | Senior Curator of Lepidoptera| Department of Life Sciences | Natural History Museum London

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From: Blanca Huertas
Sent: 23 May 2011 18:28
To: ‘tabd@ucl.ac.uk’
Subject: La investigacion en mariposas neotropicales ha cambiado para siempre

Butterfly People, please see english message below. For information on Neotropical Butterflies please register to TABDP NETWORK http://www.mailinglists.ucl.ac.uk/mailman/listinfo/tabd

**(español abajo)**

Dear friends,

As you may have seen, thanks to a collaboration between the Tropical Andean Butterfly Diversity Project (TABDP) (www.andeanbutterflies.org) and the Butterflies of America project (BoA) (www.butterfliesofamerica.com), we now have an online archive of photographs of the type specimens of neotropical butterflies:

http://www.butterfliesofamerica.com/L/Neotropical.htm

The great majority of these images are scans of print photographs taken by Gerardo Lamas over many years of research in museums throughout the world, and we are very grateful for his generosity in allowing them to be made available here. Scanning and initial databasing of the prints was completed by TABDP, supported by the Darwin Initiative, and then given to BoA to be made available online.

BoA’s Nick Grishin designed and wrote the web pages which now display the images. Numerous other people deserve acknowledgement, including the curators of the museums where these types are housed and many other members of TABDP, BoA and other lepidopterists who contributed images, time and encouragement. Please see the acknowledgements: http://www.butterfliesofamerica.com/L/Credits.htm

We are currently seeking funding to complete scanning of the remaining groups (Ithomiini, Dismorphinae and Hesperiidae). There are certainly errors within this image archive and we make no guarantees about the reliability of the data, so please read the caveats in the web page introduction. Please also read the guidelines and codes of practise on this unique opportunity: http://www.butterfliesofamerica.com/L/Cautions.htm

We hope this will prove to be a useful resource.

Kind regards,

TABDP team

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Amigos de la Red TABDP, ( y quienes aun no lo sean, por favor registrarse http://www.mailinglists.ucl.ac.uk/mailman/listinfo/tabd)

Como quiza algunos de ustedes ya se han enterado, gracias a la colaboracion entre el proyecto TABD Diversidad de las Mariposas Andinas Tropicales (www.mariposasandinas.org) y el proyecto Mariposas de America (BoA) www.butterfliesofamerica.com, podran consultar en linea, un archivo unico de las fotografias de los tipos de las mariposas tropicales:

http://www.butterfliesofamerica.com/L/Neotropical.htm

Este inigualable recurso, es producto de la digitalizacion de las fotos tomadas por nuestro colega (y maestro) Gerado Lamas durante muchos años de trabajo e investigacion en innumerables museos en el mundo. Estamos muy agradecidos por su generosidad en permitirnos hacerlos disponibles en linea y para el uso de todos. La digitalizacion y digitacion de las fotografias se completo gracias al proyecto TABD, apoyado por el Darwin Initiative. Dr Nick Grishin en sus Mariposas de America (BoA, y otros colaboradores) han disenado y escrito las paginas web en donde se encuentran las imagenes. Muchisimas otras personas merecen nuestros mas sinceros agradecimientos, incluyendo todos las instituciones y curadores de los museos donde se guardan los ejemplares tipos, todos los colaboradores del proyecto BoA y el TABDP por su tiempo y colaboracion. Todos los agradecimientos en: http://www.butterfliesofamerica.com/L/Credits.htm

Estamos buscando financiacion y su colaboracion para completar la digitalizacion de los demas grupos (Ithomiini, Dismorphinae y Hesperiidae). Por favor comuniquense con nosotros si les gustaria colaborar con este proyecto que desde hoy cambiara la historia de la investigacion de las mariposas neotropicales.

Al usar este recurso, por favor usen cautela, pues existen errores con los archivos de imagenes que esperamos se vayan corrigiendo. Igualmente, esperamos un buen codigo de practica, con profesionalismo de parte de todos al usar las imagenes. Por favor lean las recomendaciones: http://www.butterfliesofamerica.com/L/Cautions.htm

Esperamos este recurso unico sea una fuente util de consulta y una gran oportunidad para todos.

Un cordial saludo y nuestros mejores deseos,

Equipo TABD

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From mathieu.joron at cefe.cnrs.fr Thu May 17 16:46:53 2018
From: mathieu.joron at cefe.cnrs.fr (Mathieu Joron)
Date: Thu, 17 May 2018 17:46:53 +0200
Subject: [HELICONIUS] Heliconius meeting 2018 : Registration is open

Dear all

As previously advertised, we will be holding the Heliconius meeting in
Montpellier on 23-25 August. Please find below a link to the
registration form.

https://docs.google.com/forms/d/e/1FAIpQLSeSCH_GeJ5ZdN73PG3uwqoz13CWY94pxFnpPhGovtISp6aOQQ/viewform?usp=sf_link

If you are planning to come to the meeting (and even if you have said so
already by replying to my earlier email), could you please take the time
to fill the form in? You can propose a communication, and those can take
the form of a formal talk, a poster, or a discussion, a movie, a
choreography, etc… We will taylor the meeting according to the
proposed communications we receive.

I am advertising this to the Heliconius list, and to those of you who
have expressed interest, and I will post a more formal announcement on
the Lep Gen list, but there are many others in our broader community who
may not receive my emails. So, please forward this to the people in your
labs or in your network who might be interested to come, including of
course non-Heliconius biologists. To me, and to people in my group,
previous meetings have been immensely useful as they help tightening the
community, and knowing and interacting informally with people from other
labs helps at many stages of our projects. So, please encourage people
in your groups to come!

Please do not hesitate to contact us if you have any question or
suggestion, or if we can help you with planning your visit.

We hope to see you soon in Montpellier!

Best wishes

Mathieu

—
Centre d’Ecologie Fonctionnelle et Evolutive (UMR 5175)
CNRS, 1919 route de Mende, 34293 Montpellier 5, France
+33 (0)4-67-61-32-03
http://isyeb.mnhn.fr/joron
—

As if citations mattered! But still, interesting:

 

Heliconius pardalinus sergestus. Photo (c) Fraser Simpson

Dear All,

Mathieu Joron has organized the next Heliconius meeting for 23-25 Aug 2018 in Montpellier, so if you’re attending the ESEB/SSE meeting, it’s right afterwards.

Here’s a link to Mathieu’s latest message on heliconius.ucl.ac.uk.

http://www.mailinglists.ucl.ac.uk/pipermail/heliconius/2018-March.txt

In case you can’t read it, feel free to email me and I’ll sign you up for this Heliconius list server: https://www.mailinglists.ucl.ac.uk/mailman/listinfo/heliconius

Best wishes, Jim <j.mallet@ucl.ac.uk>