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Insects may acquire social information by active communication and through inadvertent social cues. In a foraging setting, the latter may indicate the presence and quality of resources. Although social learning in foraging contexts is prevalent in eusocial species, this behaviour has been hypothesized to also exist between conspecifics in non-social species with sophisticated behaviours, including Heliconius butterflies. Heliconius are the only butterfly genus with active pollen feeding, a dietary innovation associated with a specialized, spatially faithful foraging behaviour known as trap-lining. Long-standing hypotheses suggest that Heliconius may acquire trap-line information by following experienced individuals. Indeed, Heliconius often aggregate in social roosts, which could act as 'information centres', and present conspecific following behaviour, enhancing opportunities for social learning. Here, we provide a direct test of social learning ability in Heliconius using an associative learning task in which naive individuals completed a colour preference test in the presence of demonstrators trained to feed randomly or with a strong colour preference. We found no evidence that Heliconius erato, which roost socially, used social information in this task. Combined with existing field studies, our results add to data which contradict the hypothesized role of social learning in Heliconius foraging behaviour.

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Heliconius butterflies are an ideal organism for studying ecology, behavior, adaptation, and speciation. These butterflies can be found in various locations and habitats in Central and South America, where they encounter and interact with different sources of pollen, nectar, and host plants. However, there is limited knowledge on how geographic and habitat variations affect the microbiota of these insects, and whether microbial associates play a role in their ability to exploit different habitats. To date, research on the microbial communities associated with Heliconius has mainly focused on host phylogenetic signal in microbiomes or microbiome characterization in specific communities of butterflies. In this study, we characterized the microbiomes of several species and populations of Heliconius from distant locations that represent contrasting environments. We found that the microbiota of different Heliconius species is taxonomically similar but vary in abundance. Notably, this variation is associated with a major geographic barrier-the Central Cordillera of Colombia. Additionally, we confirmed that this microbiota is not associated with pollen-feeding. Therefore, it seems likely that geography shapes the abundance of microbiota that the butterfly carries, but not the taxonomic diversity of the microbial community. Based on the current evidence, the bacterial microbiota associated with Heliconius does not appear to play a beneficial role for these butterflies.

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Insect-plant interactions involve physiological adaptations by insects to secondary metabolic compounds synthetized by host plants, which are considered essential for the determination of resources partitioning of these insects. Data on such phenomena are important to understand evolutionary and ecological processes. However, climatic factors also seem to play a key role in affecting these patterns. The present study aimed to investigate the influence of seasonal variation on patterns of host plant use (Passifloraceae) by Heliconiini butterflies (Nymphalidae: Heliconiinae) at a Neotropical site in Southeastern Brazil. A total of 12 species of Heliconiini were reported, with nine of them being resident and using five species of Passiflora (Passifloraceae) as larval host plants. Three host plant species accounted for 97% of the total use, and the use varied along the seasons highlighting the plasticity boundaries in Heliconiini and possible limiting factors.

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BACKGROUND: Heliconius butterflies are widely distributed across the Neotropics and have evolved a stunning array of wing color patterns that mediate Müllerian mimicry and mating behavior. Their rapid radiation has been strongly influenced by hybridization, which has created new species and allowed sharing of color patterning alleles between mimetic species pairs. While these processes have frequently been observed in widespread species with contiguous distributions, many Heliconius species inhabit patchy or rare habitats that may strongly influence the origin and spread of species and color patterns. Here, we assess the effects of historical population fragmentation and unique biology on the origins, genetic health, and color pattern evolution of two rare and sparsely distributed Brazilian butterflies, Heliconius hermathena and Heliconius nattereri. RESULTS: We assembled genomes and re-sequenced whole genomes of eight H. nattereri and 71 H. hermathena individuals. These species harbor little genetic diversity, skewed site frequency spectra, and high deleterious mutation loads consistent with recent population bottlenecks. Heliconius hermathena consists of discrete, strongly isolated populations that likely arose from a single population that dispersed after the last glacial maximum. Despite having a unique color pattern combination that suggested a hybrid origin, we found no genome-wide evidence that H. hermathena is a hybrid species. However, H. hermathena mimicry evolved via introgression, from co-mimetic Heliconius erato, of a small genomic region upstream of the color patterning gene cortex. CONCLUSIONS: Heliconius hermathena and H. nattereri population fragmentation, potentially driven by historical climate change and recent deforestation, has significantly reduced the genetic health of these rare species. Our results contribute to a growing body of evidence that introgression of color patterning alleles between co-mimetic species appears to be a general feature of Heliconius evolution.

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Colour pattern is the main trait that drives mate recognition between Heliconius species that are phylogenetically close. However, when this cue is compromised such as in cases of mimetic, sympatric and closely related species, alternative mating signals must evolve to ensure reproductive isolation and species integrity. The closely related species Heliconius melpomene malleti and H. timareta florencia occur in the same geographical region, and despite being co-mimics, they display strong reproductive isolation. In order to test which cues differ between species, and potentially contribute to reproductive isolation, we quantified differences in the wing phenotype and the male chemical profile. As expected, the wing colour pattern was indistinguishable between the two species, while the chemical profile of the androconial and genital males' extracts showed marked differences. We then conducted behavioural experiments to study the importance of these signals in mate recognition by females. In agreement with our previous results, we found that chemical blends and not wing colour pattern drive the preference of females for conspecific males. Also, experiments with hybrid males and females suggested an important genetic component for both chemical production and preference. Altogether, these results suggest that chemicals are the major reproductive barrier opposing gene flow between these two sister and co-mimic species.

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Hybrid zones have long been of interest to biologists as natural laboratories where we can gain insight into the processes of adaptation and speciation. Repeated sampling of individual hybrid zones has been particularly useful in elucidating the dynamic balance between selection and dispersal that maintains most hybrid zones. Here, we revisit a hybrid zone between Heliconius erato butterflies in Panamá for a third time over more than 30 years. We combine a novel Bayesian extension of stepped-cline hybrid zone models with environmental data to understand the genetic and environmental causes of cline dynamics in this species. The cline has continued to move west, likely due to dominance drive, but has slowed and broadened. Environmental analyses suggest that widespread deforestation in Panamá could be leading to decreased avian predation and relaxed selection, causing the observed changes in cline dynamics.

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Sex chromosomes are disproportionately involved in reproductive isolation and adaptation. In support of such a "large-X" effect, genome scans between recently diverged populations and species pairs often identify distinct patterns of divergence on the sex chromosome compared to autosomes. When measures of divergence between populations are higher on the sex chromosome compared to autosomes, such patterns could be interpreted as evidence for faster divergence on the sex chromosome, that is "faster-X", barriers to gene flow on the sex chromosome. However, demographic changes can strongly skew divergence estimates and are not always taken into consideration. We used 224 whole-genome sequences representing 36 populations from two Heliconius butterfly clades (H. erato and H. melpomene) to explore patterns of Z chromosome divergence. We show that increased divergence compared to equilibrium expectations can in many cases be explained by demographic change. Among Heliconius erato populations, for instance, population size increase in the ancestral population can explain increased absolute divergence measures on the Z chromosome compared to the autosomes, as a result of increased ancestral Z chromosome genetic diversity. Nonetheless, we do identify increased divergence on the Z chromosome relative to the autosomes in parapatric or sympatric species comparisons that imply postzygotic reproductive barriers. Using simulations, we show that this is consistent with reduced gene flow on the Z chromosome, perhaps due to greater accumulation of incompatibilities. Our work demonstrates the importance of taking demography into account to interpret patterns of divergence on the Z chromosome, but nonetheless provides evidence to support the Z chromosome as a strong barrier to gene flow in incipient Heliconius butterfly species.

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Abstract Newly hatched caterpillars of the butterfly Heliconius erato phyllis routinely cannibalize eggs. In a manifestation of kin recognition they cannibalize sibling eggs less frequently than unrelated eggs. Previous work has estimated the heritability of kin recognition in H. erato phyllis to lie between 14 and 48%. It has furthermore been shown that the inheritance of kin recognition is compatible with a quantitative model with a threshold. Here we present the results of a preliminary study, in which we tested for associations between behavioral kin recognition phenotypes and AFLP and SSR markers. We implemented two experimental approaches: (1) a cannibalism test using sibling eggs only, which allowed for only two behavioral outcomes (cannibal and non-cannibal), and (2) a cannibalism test using two sibling eggs and one unrelated egg, which allowed four outcomes [cannibal who does not recognize siblings, cannibal who recognizes siblings, "super-cannibal" (cannibal of both eggs), and "super non-cannibal" (does not cannibalize eggs at all)]. Single-marker analyses were performed using χ2 tests and logistic regression with null markers as covariates. Results of the χ2 tests identified 72 associations for experimental design 1 and 73 associations for design 2. Logistic regression analysis of the markers found to be significant in the χ2 test resulted in 20 associations for design 1 and 11 associations for design 2. Experiment 2 identified markers that were more frequently present or absent in cannibals who recognize siblings and super non-cannibals; i.e. in both phenotypes capable of kin recognition.

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Understanding the genetic basis of phenotypic variation and the mechanisms involved in the evolution of adaptive novelty, especially in adaptive radiations, is a major goal in evolutionary biology. Here, we used whole-genome sequence data to investigate the origin of the yellow hindwing bar in the Heliconius cydno radiation. We found modular variation associated with hindwing phenotype in two narrow noncoding regions upstream and downstream of the cortex gene, which was recently identified as a pigmentation pattern controller in multiple species of Heliconius. Genetic variation at each of these modules suggests an independent control of the dorsal and ventral hindwing patterning, with the upstream module associated with the ventral phenotype and the downstream module with the dorsal one. Furthermore, we detected introgression between H. cydno and its closely related species Heliconius melpomene in these modules, likely allowing both species to participate in novel mimicry rings. In sum, our findings support the role of regulatory modularity coupled with adaptive introgression as an elegant mechanism by which novel phenotypic combinations can evolve and fuel an adaptive radiation.

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PREMISE OF THE STUDY: The ability of insect visitors to learn to manipulate complex flowers has important consequences for foraging efficiency and plant fitness. We investigated learning by two butterfly species, Danaus erippus and Heliconius erato, as they foraged on the complex flowers of Asclepias curassavica, as well as the consequences for pollination. METHODS: To examine learning with respect to flower manipulation, butterflies were individually tested during four consecutive days under insectary conditions. At the end of each test, we recorded the number of pollinaria attached to the body of each butterfly and scored visited flowers for numbers of removed and inserted pollinia. We also conducted a field study to survey D. erippus and H. erato visiting flowers of A. curassavica, as well as to record numbers of pollinaria attached to the butterflies' bodies, and surveyed A. curassavica plants in the field to inspect flowers for pollinium removal and insertion. KEY RESULTS: Learning improves the ability of both butterfly species to avoid the nonrewarding flower parts and to locate nectar more efficiently. There were no experience effects, for either species, on the numbers of removed and inserted pollinia. Heliconius erato removed and inserted more pollinia than D. erippus. For both butterfly species, pollinium removal was higher than pollinium insertion. CONCLUSION: This study is the first to show that Danaus and Heliconius butterflies can learn to manipulate complex flowers, but this learning ability does not confer benefits to pollination in A. curassavica.

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Heliconius butterflies provide good examples of both homoploid hybrid speciation and ecological speciation. In particular, examples of adaptive introgression have been detected among the subspecies of Heliconius timareta, which acquired red color pattern elements from H. melpomene. We tested whether the introgression of red wing pattern elements into H. timareta florencia might also be associated with incipient reproductive isolation (RI) from its close relative, H. timareta subsp. nov., found in the eastern Andes. No choice experiments show a 50% reduction in mating between females of H. t. subsp. nov. and males of H .t. florencia, but not in the reciprocal direction. In choice experiments using wing models, males of H. timareta subsp. nov. approach and court red phenotypes less than their own, whereas males of H. t. florencia prefer models with a red phenotype. Intrinsic postzygotic isolation was not detected in crosses between these H. timareta races. These results suggest that a color pattern trait gained by introgression is triggering RI between H. timareta subsp. nov. and H. t. florencia.

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This study reports on the embryogenesis of Heliconius erato phyllis between blastoderm formation and the prehatching larval stage. Syncytial blastoderm formation occurred approximately 2 h after egg laying (AEL) and at about 4 h, the cellular blastoderm was formed. The germ band arose from the entire length of the blastoderm, and rapidly became compacted occupying approximately two-thirds of the egg length. At about 7 h AEL, protocephalon and protocorm differentiation occurred. Continued proliferation of the germ band was followed by penetration into the yolk mass, forming a C-shaped embryo at about 10 h. Approximately 12 h AEL, the gnathal, thoracic and abdominal segments became visible. The primordium of the mouthparts and thoracic legs formed as paired evaginations, while the prolegs formed as paired lobes. At about 30 h, the embryo reversed dorsoventrally. Approximately 32 h AEL, the protocephalon and gnathal segments fused, shifting the relative position of the rudimentary appendages in this region. At about 52 h, the embryo was U-shaped in lateral view and at approximately 56 h, the bristles began evagination from the larval cuticle. Larvae hatched at about 72 h. We found that H. erato phyllis followed an embryonic pattern consistent with long-germ embryogenesis. Thus, we believe that H. erato phyllis should be classified as a long-germ lepidopteran. The study of H. erato phyllis embryogenesis provided a structural glimpse into the morphogenetic events that occur in the Heliconius egg period. This study could help future molecular approaches to understanding the evolution of Heliconius development.

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The origins of the extraordinary diversity within the Neotropics have long fascinated biologists and naturalists. Yet, the underlying factors that have given rise to this diversity remain controversial. To test the relative importance of Quaternary climatic change and Neogene tectonic and paleogeographic reorganizations in the generation of biodiversity, we examine intraspecific variation across the Heliconius cydno radiation and compare this variation to that within the closely related Heliconius melpomene and Heliconius timareta radiations. Our data, which consist of both mtDNA and genome-scan data from nearly 2250 amplified fragment length polymorphism (AFLP) loci, reveal a complex history of differentiation and admixture at different geographic scales. Both mtDNA and AFLP phylogenies suggest that H. timareta and H. cydno are probably geographic extremes of the same radiation that probably diverged from H. melpomene prior to the Pliocene-Pleistocene boundary, consistent with hypotheses of diversification that rely on geological events in the Pliocene. The mtDNA suggests that this radiation originated in Central America or the northwestern region of South America, with a subsequent colonization of the eastern and western slopes of the Andes. Our genome-scan data indicate significant admixture among sympatric H. cydno/H. timareta and H. melpomene populations across the extensive geographic ranges of the two radiations. Within H. cydno, both mtDNA and AFLP data indicate significant population structure at local scales, with strong genetic differences even among adjacent H. cydno colour pattern races. These genetic patterns highlight the importance of past geoclimatic events, intraspecific gene flow, and local population differentiation in the origin and establishment of new adaptive forms.

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As populações de Heliconius erato phyllis (Fabricius, 1775) e Heliconius ethilla narcaea Godart, 1819 foram quantificadas em uma reserva florestal de mata semi-decídual na região central do Brasil, durante o período de um ano. As subespécies apresentaram tamanho populacional similar, mas com distintos padrões. A razão sexual foi diferente entre as subespécies: H. erato phyllis apresentou mais fêmeas e H. ethilla narcaea mais machos, na maioria dos meses. Variação sazonal no tamanho dos indivíduos foi observada em ambas as populações, entretanto, a distribuição da classe etária foi diferente entre os meses e as subespécies. Assim, os resultados desse estudo demonstraram que as populações de H. erato phyllis e H. ethilla narceae apresentam semelhanças em seu tamanho, mas com propriedades e variações mensais distintas.

The populations of Heliconius erato phyllis (Fabricius, 1775) and Heliconius ethilla narcaea Godart, 1819 were monitored in a semi-deciduous forest reserve in the central region of Brazil, during the one-year period. Both subspecies presented similar population size but distinct population patterns. The sex ratio was different between the subspecies: H. erato phyllis tending to have more females and H. ethilla narceae males, in most of the observations. Seasonal variation in the adult size was observed in both populations studied, however, the distribution of the adult age structure was different between over the months and subspecies. Thus, the results of this study demonstrated that populations of H. erato phyllis and H. ethilla narceae exhibit similar population size, but distinct properties and monthly variations.

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Attempts by biogeographers to understand biotic diversification in the Amazon have often employed contemporary species distribution patterns to support particular theories, such as Pleistocene rainforest refugia, rather than to test among alternative hypotheses. Suture zones, narrow regions where multiple contact zones and hybrid zones between taxa cluster, have been seen as evidence for past expansion of whole biotas that have undergone allopatric divergence in vicariant refuges. We used coalescent analysis of mutilocus sequence data to examine population split times in 22 pairs of geminate taxa in ithomiine and heliconiine butterflies. We test a hypothesis of simultaneous divergence across a suture zone in NE Peru. Our results reveal a scattered time course of diversification in this suture zone, rather than a tight cluster of split times. Additionally, we find rapid diversification within some lineages such as Melinaea contrasting with older divergence within lineages such as the Oleriina (Hyposcada and Oleria). These results strongly reject simple vicariance as a cause of the suture zone. At the same time, observed lineage effects are incompatible with a series of geographically coincident vicariant events which should affect all lineages similarly. Our results suggest that Pleistocene climatic forcing cannot readily explain this Peruvian suture zone. Lineage-specific biological traits, such as characteristic distances of gene flow or varying rates of parapatric divergence, may be of greater importance.

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A field survey of flowering plants used as food resource by the adults of Heliconius erato phyllis (Fabricius, 1775) was carried out in four sites located in Rio Grande do Sul state, Brazil. Samples were taken in preserved areas of the Atlantic Rain and Myrtaceae forests, an Eucalyptus plantation, and an urban park. Adult feeding frequencies on flowers were registered monthly from December 1996 to May 1997, on plants located on previously marked 200 m long transects. Flowers on which H. erato phyllis fed in the field were collected, drawn and morphometrically characterized. Feeding was registered on flowers of twenty-three species, of which seventeen are new records for H. erato in Brazil . The use of a given plant varied among localities, as a function of its corresponding abundance. The most visited flowers were those of Lantana camara L. and Stachytarpheta cayennensis (Rich.) Vahl, followed by Dahliapinnata Voss in the urban site. The data suggest the existence of size and shape convergence between the proboscis and the small, tubular flowers upon which H. eratophyllis feeds. They also indicate that H. eratophyllis adults have an opportunistic nectar feeding / pollen gathering habit, using several of those flowers available in a given time and locality that fit such a morphometrical pattern. Since plant species of both primitive and derived families are used, there is no indication that phylogenetic constraints play a major role in this association, nor that color of flowers, growth pattern or size of the plants are relevant in determining their use by H. erato phyllis.

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A field survey of flowering plants used as food resource by the adults of Heliconius erato phyllis (Fabricius, 1775) was carried out in four sites located in Rio Grande do Sul state, Brazil. Samples were taken in preserved areas of the Atlantic Rain and Myrtaceae forests, an Eucalyptus plantation, and an urban park. Adult feeding frequencies on flowers were registered monthly from December 1996 to May 1997, on plants located on previously marked 200 m long transects. Flowers on which H. erato phyllis fed in the field were collected, drawn and morphometrically characterized. Feeding was registered on flowers of twenty-three species, of which seventeen are new records for H. erato in Brazil . The use of a given plant varied among localities, as a function of its corresponding abundance. The most visited flowers were those of Lantana camara L. and Stachytarpheta cayennensis (Rich.) Vahl, followed by Dahliapinnata Voss in the urban site. The data suggest the existence of size and shape convergence between the proboscis and the small, tubular flowers upon which H. eratophyllis feeds. They also indicate that H. eratophyllis adults have an opportunistic nectar feeding / pollen gathering habit, using several of those flowers available in a given time and locality that fit such a morphometrical pattern. Since plant species of both primitive and derived families are used, there is no indication that phylogenetic constraints play a major role in this association, nor that color of flowers, growth pattern or size of the plants are relevant in determining their use by H. erato phyllis.

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A field survey of flowering plants used as food resource by the adults of Heliconius erato phyllis (Fabricius, 1775) was carried out in four sites located in Rio Grande do Sul state, Brazil. Samples were taken in preserved areas of the Atlantic Rain and Myrtaceae forests, an Eucalyptus plantation, and an urban park. Adult feeding frequencies on flowers were registered monthly from December 1996 to May 1997, on plants located on previously marked 200 m long transects. Flowers on which H. erato phyllis fed in the field were collected, drawn and morphometrically characterized. Feeding was registered on flowers of twenty-three species, of which seventeen are new records for H. erato in Brazil . The use of a given plant varied among localities, as a function of its corresponding abundance. The most visited flowers were those of Lantana camara L. and Stachytarpheta cayennensis (Rich.) Vahl, followed by Dahliapinnata Voss in the urban site. The data suggest the existence of size and shape convergence between the proboscis and the small, tubular flowers upon which H. eratophyllis feeds. They also indicate that H. eratophyllis adults have an opportunistic nectar feeding / pollen gathering habit, using several of those flowers available in a given time and locality that fit such a morphometrical pattern. Since plant species of both primitive and derived families are used, there is no indication that phylogenetic constraints play a major role in this association, nor that color of flowers, growth pattern or size of the plants are relevant in determining their use by H. erato phyllis.