|Forms of Heliconius numata, H. melpomene and H. erato|
About 39, see species list in text.
Heliconius comprises a colorful and widespread genus of brush-footed butterflies commonly known as the longwings or heliconians. This genus is distributed throughout the tropical and subtropical regions of the New World, from South America as far north as the southern United States. The larvae of these butterflies eat passion flower vines (Passifloraceae). Adults exhibit bright wing color patterns which signal their distastefulness to potential predators.
Brought to the forefront of scientific attention by Victorian naturalists, these butterflies exhibit a striking diversity and mimicry, both amongst themselves and with species in other groups of butterflies and moths. The study of Heliconius and other groups of mimetic butterflies allowed the English naturalist Henry Walter Bates, following his return from Brazil in 1859, to lend support to Charles Darwin, who had found similar diversity amongst the Galápagos finches.
Model for evolutionary study
Heliconius butterflies have been a subject of many studies, due partly to their abundance and the relative ease of breeding them under laboratory conditions, but also because of the extensive mimicry that occurs in this group. From the nineteenth century to the present day, their study has helped scientists to understand how new species are formed and why nature is so diverse. In particular, the genus is suitable for the study of both Batesian mimicry and Müllerian mimicry.
Because of the type of plant material that Heliconius caterpillars favor and the resulting poisons they store in their tissues, the adult butterflies are usually unpalatable to predators. This warning is announced, to the mutual benefit of both parties, by bright colors and contrasting wing patterns, a phenomenon known as aposematism. Heliconius butterflies are thus Müllerian mimics of one another, and are also involved in Müllerian mimicry with various species of Ithomiini, Danaini, Riodinidae (Ithomeis and Stalachtis) and Acraeini as well as pericopine arctiid moths. They are probably the models for various palatable Batesian mimics, including Papilio zagreus and various Phyciodina.
Heliconius butterflies such as Heliconius numata benefit from mimicking other unpalatable species of butterfly in their local habitat, such as Melinaea, because doing so spreads the cost of educating predators. Such mimicry is termed Müllerian and may result in convergent evolution. Work has been done to try to understand the genetic changes responsible for the convergent evolution of wing patterns in comimetic species. Molecular work on two distantly related Heliconius comimics, Heliconius melpomene and Heliconius erato, has revealed that homologous genomic regions in the species are responsible for the convergence in wing patterns. Also, Supple had found evidence of two co-mimics H. erato and H. melpomene having no shared single-nucleotide polymorphisms (SNPs), which would be indicative of introgression, and hypothesized the same regulatory genes for color/pattern had comparably changed in response to the same selective forces. Similarly, molecular evidence indicates that Heliconius numata shares the same patterning homologues, but that these loci are locked into a wing patterning supergene that results in a lack of recombination and a finite set of wing pattern morphs.
One puzzle with Müllerian mimicry/convergence is that it would be predicted the butterflies to all eventually converge on the same color and pattern for the highest predator education. Instead, Heliconius butterflies are greatly diverse and even form multiple 'mimicry rings' within the same geographical area. Additional evolutionary forces are likely at work.
Heliconius butterflies are models for the study of speciation. Hybrid speciation has been hypothesized to occur in this genus and may contribute to the diverse mimicry found in Heliconius butterflies. It has been proposed that two closely related species, H. cydno and H. melpomene, hybridized to create the species H. heurippa. In addition, the clade containing Heliconius erato radiated before Heliconius melpomene, establishing the wing pattern diversity found in both species of butterfly. In a DNA sequencing comparison involving species H. m. aglope, H. timareta, and H. m. amaryllis, it was found that gene sequences around mimicry loci were more recently diverged in comparison with the rest of the genome, providing evidence for speciation by hybridization over speciation by ancestral polymorphism.
Hybridization is correlated with introgression. Results from Supple and her team have shown SNP's being polymorphic mostly around hybrid zones of a genome, and they claimed this supported the mechanism of introgression over ancestral variation for genetic material exchange for certain species. Selection factors can drive introgression to revolve around genes correlated with wing pattern and color. Research has shown introgression centering on two known chromosomes that contain mimicry alleles.
Assortive mating reproductively isolates H. heurippa from its parental species. Melo did a study on the hybrid H. heurippa to determine its mating habits regarding preference between other hybrids and its parental species. The results showed H. heurippa chose to reproduce via backcrossing, while the parental species were highly unlikely to reproduce with the backcrosses. This is significant, because hybrids' mating behavior would relatively quickly isolate itself from its parental species, and eventually form a species itself, as defined by lack of gene flow. His team also hypothesized that along with a mixed inheritance of color and pattern, the hybrids also obtained a mixed preference for mates from their parental species genes. The H. heurippa likely had a genetic attraction for other hybrids, leading to its reproductive isolation and speciation.
Although rare, Heliconius butterflies are an example of homoploid hybrid speciation, i.e. hybridization without changing the number of chromosomes. Aposematism, using warning colors, has been noted to improve species diversification, which may also contribute to the wide range of Heliconius butterflies.
Sexual selection of aposematic colors
For aposematism and mimicry to be successful in the butterflies, they must continually evolve their colours to warn predators of their unpalatability. Sexual selection is important in maintaining aposematism, as it helps to select for specific shades of colours rather than general colors. A research team used techniques to determine some the color qualities of a set of butterflies. They found that color was more vivid on the dorsal side of the butterflies than on the ventral. Also, in comparing the sexes, females appeared to have differing brightness in specific spots. It is important to select for specific colors to avoid subtle shades in any of the species involved in the mimicry. Unsuccessful warning colors will reduce the efficiency of the aposematism. To select for specific colours, neural receptors in the butterflies' brains give a disproportionate recognition and selection to those shades. To test the importance of these neural and visual cues in the butterflies, researchers conducted an experiment wherein they eliminated colours from butterflies' wings. When a colour was eliminated, the butterfly was less successful in attracting mates and therefore did not reproduce as much as its counterparts
Mating and offspring
Heliconius has evolved two forms of mating. The main form is standard sexual reproduction. Some species of Heliconius, however, have converged evolutionarily in regard to pupal mating. One species to exhibit this behavior is Heliconius charithonia. In this form of mating, the male Heliconius finds a female pupa and waits until a day before she is moulted to mate with her. With this type of mating there is no sexual selection present. H. erato has a unique mating ritual, in which males transfer anti-aphrodisiac pheromones to females after copulation so that no other males will approach the mated females. No other Lepidoptera exhibit this behavior.
Heliconius female butterflies also disperse their eggs much more slowly than other species of butterflies. They obtain their nutrients for egg production through pollen in the adult stage rather than the larval stage. Due to nutrient collection in the adult rather than larval stage, adult females have a much longer life than other species, which allows them to better disperse their eggs for survival and speciation. This form of egg production is helpful because larvae are much more vulnerable than adult stages, although they also utilize aposematism. Because many of the nutrients needed to produce eggs are obtained in the adult stage, the larval stage is much shorter and less susceptible to predation.
In order to be unpalatable, the Heliconius butterflies use cyanic characteristics, meaning they produce substances that have a cyanide group attached to them, ultimately making them harmful. Research has found that the amino acids needed to make the cyanic compounds come from feeding on pollen. Although feeding on pollen takes longer than nectar feeding, the aposematic characteristics help to warn predators away and give them more time for feeding. While Heliconius larvae feed on Passifloraceae which also have cyanic characteristics, the larvae have evolved the ability to neutralize cyanic molecules to protect them from the negative effects of the plant.
Most current researchers agree that there are some 39 Heliconius species. These are listed alphabetically here, according to Gerardo Lamas' (2004) checklist. Note that the subspecific nomenclature is incomplete for many species (there are over 2000 published names associated with the genus, many of which are subjective synonyms or infrasubspecific names).
- Heliconius Kluk, 1802
- Heliconius antiochus (Linnaeus, 1767) – Antiochus longwing
- Heliconius aoede (Hübner, )
- Heliconius astraea Staudinger, 1897
- Heliconius atthis Doubleday, 1847 – Athis longwing or false zebra longwing
- Heliconius besckei Ménétriés, 1857
- Heliconius burneyi (Hübner, 1816) – Burney's longwing
- Heliconius charithonia (Linnaeus, 1767) – zebra longwing
- Heliconius clysonymus Latreille, 1817 – Clysonymus longwing, montane longwing
- Heliconius congener Weymer, 1890
- Heliconius cydno (Doubleday, 1847) – cydno longwing
- Heliconius demeter Staudinger, 1897 – Demeter longwing
- Heliconius doris (Linnaeus, 1771) – Doris longwing
- Heliconius egeria (Cramer, 1775)
- Heliconius eleuchia Hewitson, 1853 – eleuchia longwing
- Heliconius elevatus Nöldner, 1901
- Heliconius erato (Linnaeus, 1764) – crimson-patched longwing, red postman
- Heliconius eratosignis (Joicey & Talbot, 1925)
- Heliconius ethilla (Godart, 1819) – Ethilia longwing
- Heliconius godmani Staudinger, 1882
- Heliconius hecale (Fabricius, 1775) – tiger longwing or Hecale longwing
- Heliconius hecalesia Hewitson, 1853 – five-spotted longwing
- Heliconius hecuba (Hewitson, ) – Hecuba longwing
- Heliconius hermathena (Hewitson, 1853) – Hermathena longwing
- Heliconius heurippa (Hewitson, 1853)
- Heliconius hewitsoni Staudinger, 1875
- Heliconius hierax Hewitson, 1869
- Heliconius himera Hewitson, 1867
- Heliconius hortense Guérin,  – Mexican longwing or mountain longwing
- Heliconius ismenius Latreille,  – Ismenius tiger or tiger helconian
- Heliconius lalitae Brévignon, 1996
- Heliconius leucadia (Bates, 1862) – Leucadia longwing
- Heliconius melpomene (Linnaeus, 1758) – (common) postman
- Heliconius metharme (Erichson, )
- Heliconius metis (Moreira & Mielke, 2010)
- Heliconius nattereri Felder, 1865 – Natterer's longwing
- Heliconius numata (Cramer, 1780) – Numata longwing
- Heliconius pachinus Salvin, 1871 – pachinus longwing
- Heliconius pardalinus (Bates, 1862)
- Heliconius peruvianus Felder – Peruvian longwing
- Heliconius ricini (Linnaeus, 1758) – ricini longwing
- Heliconius sapho (Drury, 1782) – Sapho longwing
- Heliconius sara (Fabricius, 1793) – Sara longwing
- Heliconius sergestus (Weymer, 1894)
- Heliconius telesiphe Doubleday, 1847 – telesiphe longwing
- Heliconius timareta (Hewitson, 1867)
- Heliconius tristero Brower, 1996
- Heliconius wallacei Reakirt, 1866 – Wallace's longwing
- Heliconius xanthocles Bates, 1862
- Wade, Nicholas (15 August 2011). "A Supergene Paints Wings for Surviving Biological War". NY Times. Retrieved 17 August 2011.
- Baxter, S W; Papa, R; Chamberlain, N; Humphray, J S; Joron, M; Morrison, C; Ffrench-Constant, R H (2008). "Convergent evolution in the genetic basis of Müllerian mimicry in Heliconius butterflies". Genetics. 180 (3): 1567–77. doi:10.1534/genetics.107.082982. PMC 2581958. PMID 18791259.
- Counterman, B A, Araujo-Perez, F, Hines, H M, Baxter, S W, Morrison, C M, Lindstrom, D P and Papa, R, 2010. Genomic hotspots for adaptation: The population genetics of Müllerian mimicry in Heliconius erato. PLOS Genetics 6:-.
- Joron, M; Papa, R; Beltran, M; Chamberlain, N; Mavarez, J; Baxter, S; Abanto, M (2006). "A conserved supergene locus controls color pattern diversity in Heliconius butterflies". PLOS Biology. 4 (10): 1831–40. doi:10.1371/journal.pbio.0040303. PMC 1570757. PMID 17002517.
- Supple, M., Hines, H., Dasmahapatra, K., Lewis J., Nielsen D., Lavoie, C., Ray, D., Salavar, C., Mcmillan, O., Counterman, B. 2103. Genomic architecture of adaptive color pattern divergence and convergence in Heliconius butterflies. Genome research (2013): gr-150615.
- Joron, M; Frezal, L; Jones, R T; Chamberlain, N L (2011). ""et al." 2011. Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry". Nature. 477 (7363): 203–08. doi:10.1038/nature10341. PMC 3717454. PMID 21841803.
- Mallet, J. & Gilbert, L. (1994). "Why are there so many mimicry rings? Correlations between habitats, behaviour, and mimicry in Heliconius butterflies". Biological Journal of the Linnean Society (1995), 55: 159-180.
- Brower A V Z (2011). "Hybrid speciation in Heliconius butterflies? A review and critique of the evidence". Genetica. 139 (2): 589–609. doi:10.1007/s10709-010-9530-4. PMC 3089819. PMID 21113790.
- Brower, Andrew V. Z. (1994). "Rapid Morphological Radiation and Convergence Among Races of the Butterfly Heliconius erato Inferred from Patterns of Mitochondrial DNA Evolution". Proceedings of the National Academy of Sciences of the United States of America. 91 (14): 6491–6495. doi:10.1073/pnas.91.14.6491. JSTOR 2364999. PMID 8022810.
- Joel Smith and Marcus R. Kronforst. "Do Heliconius Butterflies species exchange mimicry alleles?" Biology Letters. 2013 9, 20130503, published 17 July 2013.
- Nadeau, N., Martin, S., Kozak, K., Salazar, C., Dasmahapatra, K., Davey, J., Baxter, S., Blaxter, M., Mallet, J., Jiggins C. 2012. Genome-wide patterns of divergence and gene flow across a butterfly radiation. Molecular Ecology (2013) 22, 814-826.
- The Heliconius Genome Consortium. 2012. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature (2012) vol. 487.
- Mavarez, J; Salazar, C A; Bermingham, E; Salcedo, C; Jiggins, C D; Linares, M (2006). "Speciation by hybridization in Heliconius butterflies". Nature. 441 (7095): 868–71. doi:10.1038/nature04738. PMID 16778888. S2CID 2457445.
- Melo, M.; Salazar, C.; Jiggins, C.; Linares, M. (2008). "Assortative mating preferences among hybrids offer a route to hybrid speciation". Evolution. 63 (6): 1660–1665. doi:10.1111/j.1558-5646.2009.00633.x. PMID 19492995. S2CID 17250691.
- Mavarez, J.; Salazar, C.A.; Bermingham, E.; Salcedo, C.; Jiggins, C.D.; Linares, M. (2006). "Speciation by hybridization in Heliconius butterflies". Nature. 441 (7095): 868–71. doi:10.1038/nature04738. PMID 16778888. S2CID 2457445.
- Prezeczek, K; Mueller, C.; Vamosi, S.M. (2008). "The evolution of the aposematism is accompanied by increased diversification". Integrative Zoology. 3 (3): 149–156. doi:10.1111/j.1749-4877.2008.00091.x. PMID 21396063.
- Llaurens, V; Joron, M; Thery, M. (2014). "Cryptic differences in colour among Mullerian mimics: how can the visual capacities of predators and prey shape the evolution of wingcolours?". J. Evol. Biol. 27 (3): 531–540. doi:10.1111/jeb.12317. PMID 24444083. S2CID 19055696.
- Vane-Wright R.I, P.R. Ackery eds. (1984). The Biology of Butterflies. Symposium of the Royal Entomological Society of London. Number 11. Academic Press, London, U.K.
- Mavarez, J; Salazar, C; Bermingham, E; Salcedo, C; Jiggins, C; Linares, M (2006). "Speciation by hybridization in the Heliconius butterflies". Nature. 441 (7095): 868–871. doi:10.1038/nature04738. PMID 16778888. S2CID 2457445.
- Sourakov, Andrei (2008). "Pupal Mating in Zebra Longwing (Heliconius charithonia): Photographic Evidence". News of the Lepidopterists' Society. 50 (1): 26–32.
- Gilbert, Lawrence E. (1976). "Postmating Female Odor in Heliconius Butterflies: A Male-Contributed Antiaphrodisiac?". Science. 193 (4251): 419–420. doi:10.1126/science.935877. JSTOR 1742803. PMID 935877.
- Gilbert, L.E. (1972). "Feeding and Reproductive Biology of Heliconius Butterflies". Proc. Natl. Acad. Sci. 69 (6): 1403–1407. doi:10.1073/pnas.69.6.1403. PMC 426712. PMID 16591992.
- Nahrstedt A, R.H. Davis. 1980. The occurrence of the cyanoglucosides linamarin and lotaustralin, in Acraea and Heliconius butterflies. Comp. Biochem. Physiol.68B:575-577.
- Price P.W., T.M. Lewinsohn, G.W. Fernandes, W.W. Benson eds. 1991. Plant- Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions. John Wiley and Sons, Inc, New. York, United States.
- Lamas, G (Ed), 2004. Atlas of Neotropical Lepidoptera. Checklist: Part 4A Hesperioidea – Papiionoidea. Gainesville, Scientific Publishers/Association of Tropical Lepidoptera.
- Heliconiini Archived 2010-07-11 at the Wayback Machine, Nymphalidae Study Group website
- Heliconius at Markku Savela's Lepidoptera and Some Other Life Forms
- Heliconius, Neotropical Butterflies
- Rosser, Neil; Freitas, André V. L.; Huertas, Blanca; Joron, Mathieu; Lamas, Gerardo; Mérot, Claire; Simpson, Fraser; Willmott, Keith R.; Mallet, James; Dasmahapatra, Kanchon K. (2019). "Cryptic speciation associated with geographic and ecological divergence in two Amazonian Heliconius butterflies". Zoological Journal of the Linnean Society. 186 (1): 233–249. doi:10.1093/zoolinnean/zly046.
- Holzinger, H. and Holzinger, R, 1994. Heliconius and related genera. Sciences Nat, Venette, pp. 1–328, pl. 1–51 
- Kapan, D D (2001). "Three-butterfly system provides a field test of Müllerian mimicry". Nature. 409 (6818): 338–40. doi:10.1038/35053066. PMID 11201741. S2CID 4414609.
- Kronforst, M R; Young, L G; Blume, L M; Gilbert, L E (2006). "Multilocus analyses of admixture and introgression among hybridizing Heliconius butterflies". Evolution. 60 (6): 1254–68. doi:10.1111/j.0014-3820.2006.tb01203.x. PMID 16892975. S2CID 17899934.
- Mallet, J; Beltrán, M; Neukirchen, W; Linares, M (2007). "Natural hybridization in heliconiine butterflies: The species boundary as a continuum". BMC Evol Biol. 7: 28. doi:10.1186/1471-2148-7-28. PMC 1821009. PMID 17319954.
|Wikimedia Commons has media related to Heliconius.|
|Wikispecies has information related to Heliconius.|
- Heliconius Research Worldwide
- Michel Cast La La diversité des Heliconius
- Tree of Life: Heliconius
- Checklist of Heliconiini with links to maps
- Neil Rosser et al.: Source geographic distribution data for the species 
- Rosser, N; Phillimore, AB; Huertas, B; Willmott, KR; Mallet, J (2012). "Testing historical explanations for gradients in species richness in heliconiine butterflies of tropical America". Biological Journal of the Linnean Society. 105 (3): 479–497. doi:10.1111/j.1095-8312.2011.01814.x.