Heliconius

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Heliconius
Heliconius mimicry.png
Forms of Heliconius numata , H. melpomene and H. erato
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Arthropoda
Class: Insecta
Order: Lepidoptera
Family: Nymphalidae
Tribe: Heliconiini
Genus: Heliconius
Kluk, 1780
Type species
Papilio charithonia
Species

About 39, see species list in text.

Synonyms
  • AjantisHübner, 1816
  • ApostraphiaHübner, 1816
  • BlanchardiaBuchecker, 1880 (non Castelnau, 1875: preoccupied)
  • CrenisHübner, 1821
  • HeliconiaGodart 1819
  • LaparusBillberg, 1820
  • MigonitisHübner, 1816 (non Rafinesque, 1815: preoccupied)
  • NerudaTurner, 1976
  • PhlogrisHübner, 1825
  • Podalirius Gistel, 1848
  • SuniasHübner, 1816
  • SicyoniaHübner, 1816

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.

Contents

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. [1] 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.

Convergence

Heliconius butterflies such as Heliconius numata are famous practitioners of Müllerian mimicry, and benefit from mimicking other unpalatable species of butterfly in their local habitat, such as Melinaea . This type of mimicry typically results in convergent evolution, whereby many (sometimes unrelated) species become protected by similar patterns or coloration. This is a distinct strategy from the better-known Batesian mimicry. In Batesian mimics defensive coloration or patterns are a bluff, mimicking those of actually poisonous or foul-tasting species. In Müllerian mimicry all species of the set have honest warnings, but the similarity between members of a set allows a single encounter between a predator and one member of the set to deter that predator in all future encounters with all members of the set. In this way multiple, often unrelated species, effectively cooperate with one another to educate their mutual predators. [1]

Work has been done 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. [2] [3] [4] 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. [5] 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. [6]

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. [7]

Speciation

Wing pattern mimicry among various Heliconius species. Wing pattern mimicry among species in the melpomene-cydno-silvaniform clade and the erato-sapho-sara clade of Heliconius species - Fevo -08-00221-g001.jpg
Wing pattern mimicry among various Heliconius species.

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. [8] 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. [9] 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. [10]

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. [5] Selection factors can drive introgression to revolve around genes correlated with wing pattern and color. [11] Research has shown introgression centering on two known chromosomes that contain mimicry alleles. [12]

Assortive mating reproductively isolates H. heurippa from its parental species. [13] 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. [14]

Heliconius butterflies provide examples of a probably rare form of speciation, homoploid hybrid speciation, i.e. hybridization without changing the number of chromosomes. For various reasons, while it remains a good example of introgression of a color trait involved in mating from H. melpomene, H. heurippa is no longer regarded as a good example of hybrid speciation [15] ; the problem is that H. heurippa is today regarded as little more than a local form of the more widespread H. timareta, which occurs along the eastern slopes of the Andes between Colombia and Peru and whose divergent populations also have many other examples of different color pattern introgression from different geographic forms of H. melpomene. It is unlikely that H. heurippa is reproductively isolated enough from its "H. timareta" parent to warrant status as a species in its own right.

However, at least two more recent excellent examples of homoploid hybrid speciation have cropped up in Heliconius. Firstly, H. hecalesia is almost certainly an ancient hybrid species between H. telesiphe (+ H. clysonymus + H. hortense) and the H. erato + H. himera lineages. [16] [17] A more recent case is Heliconius elevatus, which has been shown to be a hybrid species between H. melpomene and H. pardalinus. [18]

Sexual selection of aposematic colors

Aposematism, using warning colors, has been noted to improve species diversification, which may also contribute to the wide range of Heliconius butterflies. [19]

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. [20] 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. [21] 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. [22]

Sexual Selection of Pheromones

In order to attract mates female Heliconius secrete pheromones from a yellow like sac that they secrete the scent to appear more attractive to the males. They found that typically it is virgin female Heliconius that secrete these pheromones, The males are able to attach themselves using their denticles to these secretion sacs during mating in order to ensure secretion. Pheromones are vital when it comes to mate choice it determines the more likely chance that there will be a success in mating between the Heliconius. There is an reproductive isolation between populations so while mates are attracted by pheromones they still will choose to similar patterned winged Heliconius. [23]

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 . [24] 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. [25]

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. [26] 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. [26]

Cyanogenic glycosides as a defence

In order to be unpalatable, the Heliconius butterflies use cyanogenic 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. [27] Although feeding on pollen takes longer than nectar feeding, the aposematic characteristics help to warn predators away and give them more time for feeding. [26] While Heliconius larvae feed on Passifloraceae which also have cyanogenic characteristics, the larvae have evolved the ability to neutralize cyanic molecules to protect them from the negative effects of the plant. [28]

Species

Tiger longwing (Heliconius hecale) Heliconius hecale.JPG
Tiger longwing (Heliconius hecale)
Numata longwing (Heliconius numata) Numata Longwing with Red Postman.jpg
Numata longwing (Heliconius numata)
Heliconius hewitsoni Heliconius hewitsoni.jpg
Heliconius hewitsoni
Sara longwing (Heliconius sara) Butterfly panama.jpg
Sara longwing (Heliconius sara)
Doris longwing (Heliconius doris) Laparus doris viridis (top).jpg
Doris longwing (Heliconius doris)

Most current researchers agree that there are some 45-50 Heliconius species. These are listed alphabetically here, according to Gerardo Lamas' (2017) updated checklist. [29] [30] 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). [31] [32] [33] Additional useful images of these butterflies, largely correctly identified to subspecies, can be found in various websites. [34] [35]

Related Research Articles

<span class="mw-page-title-main">Hybrid (biology)</span> Offspring of cross-species reproduction

In biology, a hybrid is the offspring resulting from combining the qualities of two organisms of different varieties, subspecies, species or genera through sexual reproduction. Generally, it means that each cell has genetic material from two different organisms, whereas an individual where some cells are derived from a different organism is called a chimera. Hybrids are not always intermediates between their parents such as in blending inheritance, but can show hybrid vigor, sometimes growing larger or taller than either parent. The concept of a hybrid is interpreted differently in animal and plant breeding, where there is interest in the individual parentage. In genetics, attention is focused on the numbers of chromosomes. In taxonomy, a key question is how closely related the parent species are.

<span class="mw-page-title-main">Mimicry</span> Evolutionary strategy

In evolutionary biology, mimicry is an evolved resemblance between an organism and another object, often an organism of another species. Mimicry may evolve between different species, or between individuals of the same species. In the simplest case, as in Batesian mimicry, a mimic resembles a model, so as to deceive a dupe, all three being of different species. A Batesian mimic, such as a hoverfly, is harmless, while its model, such as a wasp, is harmful, and is avoided by the dupe, such as an insect-eating bird. Birds hunt by sight, so the mimicry in that case is visual, but in other cases mimicry may make use of any of the senses. Most types of mimicry, including Batesian, are deceptive, as the mimics are not harmful, but Müllerian mimicry, where different harmful species resemble each other, is honest, as when species of wasps and of bees all have genuinely aposematic warning coloration. More complex types may be bipolar, involving only two species, such as when the model and the dupe are the same; this occurs for example in aggressive mimicry, where a predator in wolf-in-sheep's-clothing style resembles its prey, allowing it to hunt undetected. Mimicry is not limited to animals; in Pouyannian mimicry, an orchid flower is the mimic, resembling a female bee, its model; the dupe is the male bee of the same species, which tries to copulate with the flower, enabling it to transfer pollen, so the mimicry is again bipolar. In automimicry, another bipolar system, model and mimic are the same, as when blue lycaenid butterflies have 'tails' or eyespots on their wings that mimic their own heads, misdirecting predator dupes to strike harmlessly. Many other types of mimicry exist.

<span class="mw-page-title-main">Heliconiinae</span> Subfamily of butterfly family Nymphalidae

The Heliconiinae, commonly called heliconians or longwings, are a subfamily of the brush-footed butterflies. They can be divided into 45–50 genera and were sometimes treated as a separate family Heliconiidae within the Papilionoidea. The colouration is predominantly reddish and black, and though of varying wing shape, the forewings are always elongated tipwards, hence the common name.

<span class="mw-page-title-main">Viceroy (butterfly)</span> Species of butterfly

The viceroy is a North American butterfly. It was long thought to be a Batesian mimic of the monarch butterfly, but since the viceroy is also distasteful to predators, it is now considered a Müllerian mimic instead.

<i>Heliconius charithonia</i> Species of butterfly

Heliconius charithonia, the zebra longwing or zebra heliconian, is a species of butterfly belonging to the subfamily Heliconiinae of the family Nymphalidae. It was first described by Carl Linnaeus in his 1767 12th edition of Systema Naturae. The boldly striped black and white wing pattern is aposematic, warning off predators. It is the state butterfly of Florida.

<span class="mw-page-title-main">Müllerian mimicry</span> Mutually beneficial mimicry of strongly defended species

Müllerian mimicry is a natural phenomenon in which two or more well-defended species, often foul-tasting and sharing common predators, have come to mimic each other's honest warning signals, to their mutual benefit. The benefit to Müllerian mimics is that predators only need one unpleasant encounter with one member of a set of Müllerian mimics, and thereafter avoid all similar coloration, whether or not it belongs to the same species as the initial encounter. It is named after the German naturalist Fritz Müller, who first proposed the concept in 1878, supporting his theory with the first mathematical model of frequency-dependent selection, one of the first such models anywhere in biology.

<span class="mw-page-title-main">Aposematism</span> Honest signalling of an animals powerful defences

Aposematism is the advertising by an animal, whether terrestrial or marine, to potential predators that it is not worth attacking or eating. This unprofitability may consist of any defenses which make the prey difficult to kill and eat, such as toxicity, venom, foul taste or smell, sharp spines, or aggressive nature. These advertising signals may take the form of conspicuous coloration, sounds, odours, or other perceivable characteristics. Aposematic signals are beneficial for both predator and prey, since both avoid potential harm.

<span class="mw-page-title-main">Introgression</span> Transfer of genetic material from one species to another

Introgression, also known as introgressive hybridization, in genetics is the transfer of genetic material from one species into the gene pool of another by the repeated backcrossing of an interspecific hybrid with one of its parent species. Introgression is a long-term process, even when artificial; it may take many hybrid generations before significant backcrossing occurs. This process is distinct from most forms of gene flow in that it occurs between two populations of different species, rather than two populations of the same species.

<i>Heliconius erato</i> Species of butterfly

Heliconius erato, or the red postman, is one of about 40 neotropical species of butterfly belonging to the genus Heliconius. It is also commonly known as the small postman, the red passion flower butterfly, or the crimson-patched longwing. It was described by Carl Linnaeus in his 1758 10th edition of Systema Naturae.

<i>Heliconius cydno</i> Species of butterfly

Heliconius cydno, the cydno longwing, is a nymphalid butterfly that ranges from Mexico to northern South America. It is typically found in the forest understory and deposits its eggs on a variety of plants of the genus Passiflora. It is a member of the Heliconiinae subfamily of Central and South America, and it is the only heliconiine that can be considered oligophagous. H. cydno is also characterized by hybridization and Müllerian mimicry. Wing coloration plays a key role in mate choice and has further implications in regards to sympatric speciation. Macrolide scent gland extracts and wing-clicking behavior further characterize this species.

<span class="mw-page-title-main">Hybrid speciation</span> Form of speciation involving hybridization between two different species

Hybrid speciation is a form of speciation where hybridization between two different species leads to a new species, reproductively isolated from the parent species. Previously, reproductive isolation between two species and their parents was thought to be particularly difficult to achieve, and thus hybrid species were thought to be very rare. With DNA analysis becoming more accessible in the 1990s, hybrid speciation has been shown to be a somewhat common phenomenon, particularly in plants. In botanical nomenclature, a hybrid species is also called a nothospecies. Hybrid species are by their nature polyphyletic.

<i>Heliconius melpomene</i> Species of butterfly

Heliconius melpomene, the postman butterfly, common postman or simply postman, is a brightly colored, geographically variable butterfly species found throughout Central and South America. It was first described by Carl Linnaeus in his 1758 10th edition of Systema Naturae. Its coloration coevolved with another member of the genus, H. erato as a warning to predators of its inedibility; this is an example of Müllerian mimicry. H. melpomene was one of the first butterfly species observed to forage for pollen, a behavior that is common in other insect groups but rare in butterflies. Because of the recent rapid evolutionary radiation of the genus Heliconius and overlapping of its habitat with other related species, H. melpomene has been the subject of extensive study on speciation and hybridization. These hybrids tend to have low fitness as they look different from the original species and no longer exhibit Müllerian mimicry.

<i>Heliconius ismenius</i> Species of butterfly

Heliconius ismenius, the Ismenius tiger or tiger heliconian, is a butterfly of the family Nymphalidae found in Central America and northern South America. They are abundant as far south as Ecuador and Venezuela and as far north as southern Mexico, Guatemala and Belize. H. ismenius are more commonly called the tiger-striped long wing butterfly. H. ismenius's nickname is derived from its long wing structure as well as the beautiful burnt orange and black stripes. Pierre André Latreille, a French zoologist, described Heliconius ismenius in 1817. H. ismenius resembles a number of other butterflies, an example of Müllerian mimicry.

<i>Heliconius heurippa</i> Species of butterfly

Heliconius heurippa is a butterfly of the genus Heliconius that is believed by some scientists to be a separate species from—but a hybrid of—the species Heliconius cydno and Heliconius melpomene, making H. heurippa an example of hybrid speciation.

<i>Heliconius numata</i> Species of butterfly

Heliconius numata, the Numata longwing, is a brush-footed butterfly species belonging to the family Nymphalidae, subfamily Heliconiinae.

<span class="mw-page-title-main">Ecological speciation</span>

Ecological speciation is a form of speciation arising from reproductive isolation that occurs due to an ecological factor that reduces or eliminates gene flow between two populations of a species. Ecological factors can include changes in the environmental conditions in which a species experiences, such as behavioral changes involving predation, predator avoidance, pollinator attraction, and foraging; as well as changes in mate choice due to sexual selection or communication systems. Ecologically-driven reproductive isolation under divergent natural selection leads to the formation of new species. This has been documented in many cases in nature and has been a major focus of research on speciation for the past few decades.

<i>Heliconius sapho</i> Species of butterfly

Heliconius sapho, the Sapho longwing, is a butterfly of the family Nymphalidae. It was described by Dru Drury in 1782. It is found from Mexico southward to Ecuador.

<span class="mw-page-title-main">Evo-devo gene toolkit</span>

The evo-devo gene toolkit is the small subset of genes in an organism's genome whose products control the organism's embryonic development. Toolkit genes are central to the synthesis of molecular genetics, palaeontology, evolution and developmental biology in the science of evolutionary developmental biology (evo-devo). Many of them are ancient and highly conserved among animal phyla.

<i>Heliconius eleuchia</i> Species of butterfly

Heliconius eleuchia, the white-edged longwing, is a species of Heliconius butterfly described by William Chapman Hewitson in 1853.

Eukaryote hybrid genomes result from interspecific hybridization, where closely related species mate and produce offspring with admixed genomes. The advent of large-scale genomic sequencing has shown that hybridization is common, and that it may represent an important source of novel variation. Although most interspecific hybrids are sterile or less fit than their parents, some may survive and reproduce, enabling the transfer of adaptive variants across the species boundary, and even result in the formation of novel evolutionary lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species genomes with no increase in chromosome number.

References

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  23. ↑ Darragh, Kathy; Vanjari, Sohini; Mann, Florian; Gonzalez-Rojas, Maria F.; Morrison, Colin R.; Salazar, Camilo; Pardo-Diaz, Carolina; Merrill, Richard M.; McMillan, W. Owen; Schulz, Stefan; Jiggins, Chris D. (2017-11-07). "Male sex pheromone components in Heliconius butterflies released by the androconia affect female choice". PeerJ. 5: e3953. doi: 10.7717/peerj.3953 . ISSN   2167-8359. PMC   5680698 . PMID   29134139.
  24. ↑ Sourakov, Andrei (2008). "Pupal Mating in Zebra Longwing (Heliconius charithonia): Photographic Evidence". News of the Lepidopterists' Society. 50 (1): 26–32.
  25. ↑ Gilbert, Lawrence E. (1976). "Postmating Female Odor in Heliconius Butterflies: A Male-Contributed Antiaphrodisiac?". Science. 193 (4251): 419–420. Bibcode:1976Sci...193..419G. doi:10.1126/science.935877. JSTOR   1742803. PMID   935877.
  26. 1 2 3 Gilbert, L.E. (1972). "Feeding and Reproductive Biology of Heliconius Butterflies". Proc. Natl. Acad. Sci. 69 (6): 1403–1407. Bibcode:1972PNAS...69.1403G. doi: 10.1073/pnas.69.6.1403 . PMC   426712 . PMID   16591992.
  27. ↑ 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.
  28. ↑ 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.
  29. ↑ Lamas, G (Ed), 2004. Atlas of Neotropical Lepidoptera. Checklist: Part 4A Hesperioidea – Papiionoidea. Gainesville, Scientific Publishers/Association of Tropical Lepidoptera.
  30. ↑ Lamas, G. & Jiggins, C. 2017. Chapter 12. Taxonomic list. pp. 214-244 in The Ecology and Evolution of Heliconius Butterflies. Oxford, Oxford University Press.
  31. ↑ Niklas Wahlberg. "Heliconiini". Archived from the original on 14 June 2024.
  32. ↑ Savela, Markku. "Heliconius". Lepidoptera and Some Other Life Forms.
  33. ↑ "Heliconiinae". Neotropical Butterflies.
  34. ↑ Demaio, Massimo, "Heliconius Butterflies", heliconius.net, retrieved 23 June 2024
  35. ↑ Cast, Michel. "La Diversité des Heliconius" . Retrieved 23 June 2024.
  36. ↑ 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 .

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