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277 results for “Heliconius”
Quantifying visual acuity in Heliconius butterflies
<p><em>Heliconius</em> butterflies are well-known for their colourful wing patterns, which advertise distastefulness to potential predators and are used during mate choice. However, the relative importance of different aspects of these signals will depend on the visual abilities of <em>Heliconius</em> and their predators. Previous studies have investigated colour sensitivity and neural anatomy, but visual acuity (the ability to perceive detail) has not been studied in these butterflies. Here, we provide the first estimate of visual acuity in Heliconius: from a behavioural optomotor assay, we found that mean visual acuity = 0.49 cycles-per-degree (cpd), with higher acuity in males than females. We also examined eye morphology and report more ommatidia in male eyes. Finally, we estimated how visual acuity affects <em>Heliconius</em> visual perception compared to a potential avian predator. Whereas the bird predator maintained high resolving power, <em>Heliconius</em> lost the ability to resolve detail at greater distances, though colours may remain salient. These results will inform future studies of <em>Heliconius</em> wing pattern evolution, as well as other aspects in these highly visual butterflies, which have emerged as an important system in studies of adaptation and speciation.</p>
Movement, translocation and MRR data for Heliconius butterflies
<p class="Normal1"><span>Site fidelity plays an important role in increasing foraging efficiency, particularly when food resources are reliable. In insects, site fidelity has largely been studied in Hymenopteran species, which consistently return to their nest site after foraging bouts. In butterflies, evidence of foraging site fidelity are limited but may be present in species with specific foraging specialisations, such as <i>Heliconius</i>, which have a derived foraging behaviour centred around active pollen feeding. Unlike many Hymenoptera, <i>Heliconius</i> are neither eusocial nor nesting species, positioning them as a peculiar case where foraging site fidelity may occur in the absence of any central nest-like structure. However, to date, existing studies do not consider low dispersal as an alternative to site fidelity. In this study, we use a mark-release-recapture experiment to test whether individuals of two <i>Heliconius </i>species exhibit true site fidelity. We further test this fidelity by measuring flight orientation during a translocation experiment, and by recapturing translocated butterflies to identify whether individuals return to their site of origin. We found that non-translocated butterflies display extreme stability in site choice, and translocated butterflies consistently return to their site of origin, rapidly orientating towards their home site upon release. This suggests site fidelity in <i>Heliconius </i>is not solely explained by low dispersal, but is a response to the distribution and stability in ecological resources. We further note that the ability to return to home sites when artificially dispersed suggests a sophisticated ability to navigate to specific spatial goals. Our study provides insights into the <span>ecological drivers of site fidelity, a novel example distinct from nest building or group living, and opens an avenue of new research on navigational mechanisms in insects.</span></span></p>
Divergence in Heliconius flight behaviour is associated with local adaptation to different forest structures
<p>Micro-habitat choice plays a major role in shaping local patterns of biodiversity. In butterflies, stratification in flight height has an important role in maintaining community diversity. The speciation in <em>Heliconius</em> butterflies is often associated with strong assortative mating, but ecological isolation and local adaptation is also considered essential. Despite its presumed importance, the role of behavioural shifts in early stages of speciation in response to differences in habitat structure is yet to be established. Here, we investigated variation in flight height behaviour in two closely related species, <em>H. erato cyrbia</em> and <em>H. himera</em>, which produce viable hybrids but are isolated across an environmental gradient, spanning lowland wet forest to high altitude scrub forest. We show that the two species fly at different heights in the wild, and demonstrate that this can be explained by differences in the vertical distribution of plant resources. We subsequently explored whether this divergence in flight height has a genetic component using common garden experiments. In both the wild and captivity, <em>H. himera</em> choose to fly lower and feed at lower positions, mirroring differences in resource availability in the wild. We suggest that this shift in foraging behaviour may reflect local adaptation to divergent forest structures highlighting the role of behaviour during early stages of speciation.</p>
Data condition dependence in biosynthesized chemical defenses of an aposematic and mimetic Heliconius butterfly
<p><span>Aposematic animals advertise their toxicity or unpalatability with bright warning coloration. However, acquiring and maintaining chemical defenses can be energetically costly, and consequent associations with other important traits could shape chemical defense evolution. Here, we have tested whether chemical defenses are involved in energetic trade-offs with other traits, or whether the levels of chemical defenses are condition dependent, by studying associations between biosynthesized cyanogenic toxicity and a suite of key life-history and fitness traits in a <em>Heliconius </em>butterfly under a controlled laboratory setting. <em>Heliconius </em>butterflies are well known for the diversity of their warning color patterns and widespread mimicry, and can both sequester the cyanogenic glucosides of their <em>Passiflora </em>host plants and biosynthesize these toxins <em>de novo</em>. We find energetically costly life-history traits to be either unassociated or to show a general positive association with biosynthesized cyanogenic toxicity. More toxic individuals developed faster, had higher mass as adults, and a tendency for increased lifespan and fecundity. These results thus indicate that toxicity level of adult butterflies may be dependent on individual condition, influenced by genetic background or earlier conditions, with maternal effects as one strong candidate mechanism. Additionally, toxicity was higher in older individuals, consistent with previous studies indicating accumulation of toxins with age. As toxicity level at death was independent of lifespan, cyanogenic glucoside compounds may have been recycled to release resources relevant for longevity in these long-living butterflies. Understanding the origins and maintenance of variation in defenses is necessary in building a more complete picture of factors shaping the evolution of aposematic and mimetic systems.</span></p>
Data From: Exploitation of an ancestral pheromone biosynthetic pathway contributes to diversification in Heliconius butterflies
<p class="MsoNormal"><span>During courtship, male butterflies produce androconial secretions containing male sex pheromones (MSPs) that communicate species identity and affect female choice. MSPs are thus likely candidates as reproductive barriers, yet their role in speciation remains poorly studied. Although <em>Heliconius </em>butterflies are a model system in speciation, their MSPs have not been investigated from a macroevolutionary perspective. We use GC-MS to characterise male androconial secretions in 33 of the 69 species in the Heliconiini tribe. We found these blends to be species-specific, consistent with a role in reproductive isolation. We detected a burst in blend diversification rate at the most speciose genus,<em> Heliconius</em>; a consequence of <em>Heliconius</em> and <em>Eueides</em> species using a fatty acid metabolic pathway to unlock more complex blends than basal Heliconiini species, whose secretions are dominated by plant derivatives. A comparison of 10 sister species pairs demonstrates a striking positive correlation between blend dissimilarity and range overlap, consistent with a scenario of character displacement or reinforcement in sympatry. These results demonstrate for the first time that MSP diversification can promote reproductive isolation across this group of butterflies, showcasing how re-activation of an ancestral trait, the co-option of the fatty acid metabolic pathway for pheromone production, can facilitate rapid speciation. </span></p>
Scale-dependent environmental effects on phenotypic distributions in Heliconius butterflies
<p>Examining how environmental factors influence phenotypic distribution might provide valuable information about local adaptation, divergence, and speciation. The red-yellow Müllerian mimicry ring of <em>Heliconius</em> butterflies displays a wide range of color patterns across the Neotropics and is involved in several hybrid zones, making it an excellent system to study color phenotypic distribution. Using a multiscale distribution strategy, we studied whether different phenotypes of the distantly related species <em>H. erato</em> and <em>H. melpomene,</em> belonging to the red-yellow mimetic ring, are associated with different environmental conditions. We show that environmental gradients (particularly heat and precipitation factors) drive <em>Heliconius</em> phenotypic distributions, but that phenotype and environmental correlations vary with spatial scale. While co-mimics are frequently found in similar environments at a broad scale, patterns at the local level are not necessarily consistent (different variables are the best predictors of phenotypic occurrence in different areas) or congruent (co-mimic pairs show distinct associations with the environment). Thus, large-scale analysis may help to identify how environmental heterogeneity influences broad mimic phenotypic distributions, but local studies are needed to understand the context-dependent biotic, abiotic, and historical mechanisms that drive finer-scale phenotypic shifts.</p>
Behavioural changes in aposematic Heliconius melpomene butterflies in response to their predatory bird calls
<p>Prey-predator interactions have resulted in the evolution of many anti-predatory traits. One of them is the ability of prey to listen to predators and avoid them. Although prey anti-predatory behavioural responses to predator auditory cues are well described in a wide range of taxa, studies on whether butterflies change their behaviours in response to their predatory calls are lacking. <em>Heliconius </em>butterflies are unpalatable and form Müllerian mimicry rings as morphological defence strategies against their avian predators. Like many other butterflies in the <em>Nymphalidae </em>family, some <em>Heliconius </em>butterflies possess auditory organs, which are hypothesized to assist with predator detection. Here we test whether <em>Heliconius melpomene </em>changes their behaviour in response to their predatory bird calls by observing the behaviour of male and female <em>H. m. plessini </em>exposed to calls of <em>Heliconius</em> avian predators: rufous-tailed jacamar, migratory Eastern kingbird, and resident tropical kingbird. We also exposed them to the calls of the toco toucan, a frugivorous bird as a control bird call, and an amplified greenhouse background noise as a noise control. We found that individuals<em> </em>changed their behaviour in response to Jacamar calls only. Males increased their walking and fluttering behaviour, while females did not change their behaviour during the playback of the jacamar call. Intersexual behaviours like courtship, copulation, and abdomen lifting did not change in response to bird calls. Our findings suggest that despite having primary predatory defences like toxicity and being in a mimicry ring, <em>H. m. plessini </em>butterflies changed their behaviour in response to predator calls. Furthermore, this response was predator-specific, as <em>H. m. plesseni</em> did not respond to either the Eastern kingbird or the tropic kingbird calls. This suggests that <em>Heliconius</em> butterflies may be able to differentiate predatory calls, and potentially the birds associated with those calls.</p>
Full-likelihood genomic analysis clarifies a complex history of species divergence and introgression: the example of the erato-sara group of Heliconius butterflies
<p>Introgressive hybridization plays a key role in adaptive evolution and species diversification in many groups of species. However, frequent hybridization and gene flow between species make estimation of the species phylogeny and key population parameters challenging. Here, we show that by accounting for phasing and using full-likelihood methods, introgression histories and population parameters can be estimated reliably from whole-genome sequence data. We employ the multispecies coalescent (MSC) model with and without gene flow to infer the species phylogeny and cross-species introgression events using genomic data from six members of the <i>erato</i>-<i>sara</i> clade of <i>Heliconius</i> butterflies. The methods naturally accommodate random fluctuations in genealogical history across the genome due to deep coalescence. To avoid heterozygote phasing errors in haploid sequences commonly produced by genome assembly methods, we process and compile unphased diploid sequence alignments and use analytical methods to average over uncertainties in heterozygote phase resolution. There is robust evidence for introgression across the genome, both among distantly related species deep in the phylogeny and between sister species in shallow parts of the tree. We obtain chromosome-specific estimates of key population parameters such as introgression directions, times and probabilities, as well as species divergence times and population sizes for modern and ancestral species. We confirm ancestral gene flow between the <i>sara</i> clade and an ancestral population of <i><span>H. telesiphe</span></i>, a likely hybrid speciation origin for <i>H. hecalesia</i>, and gene flow between the sister species <i><span>H. erato</span></i><span> and <i>H. himera</i></span>. Inferred introgression among ancestral species also explains the history of two chromosomal inversions deep in the phylogeny of the group. This study illustrates how a full-likelihood approach based on the multispecies coalescent makes it possible to extract rich historical information of species divergence and gene flow from genomic data.</p>
Cortex cis-regulatory switches establish scale colour identity and pattern diversity in Heliconius
<p></p><p>In Heliconius butterflies, wing pattern diversity is controlled by a few genes of large effect that regulate colour pattern switches between morphs and species across a large mimetic radiation. One of these genes, cortex, has been repeatedly associated with colour pattern evolution in butterflies. Here we carried out CRISPR knock-outs in multiple Heliconius species and show that cortex is a major determinant of scale cell identity. Chromatin accessibility profiling and introgression scans identified cis-regulatory regions associated with discrete phenotypic switches. CRISPR perturbation of these regions in black hindwing genotypes recreated a yellow bar, revealing their spatially limited activity. In the H. melpomene/timareta lineage, the candidate CRE from yellow-barred phenotype morphs is interrupted by a transposable element, suggesting that cis-regulatory structural variation underlies these mimetic adaptations. Our work shows that cortex functionally controls scale colour fate and that its cis-regulatory regions control a phenotypic switch in a modular and pattern-specific fashion.</p><p></p>
Heliconius erato cyrbia, Cook Islands (New Zealand) 2016, 2019, 2021
<p>EN:</p> <p>This upload contains photographs taken by Amin Ghane and Gabriela Montejo-Kovacevich in the Butterfly Genetics Group at the University of Cambridge from the June/July/August (CAM045001-CAM045330) in three batches, indicated in the csv table. These two batches might have slightly different zoom/light settings.</p> <p>This batch contains Quentin Paynter and Gabriela Montejo-Kovacevich specimen collection from the Cook Islands, wild Heliconius erato cyrbia.<br> <br> They have a colour standard for calibration. Information on the individual IDs can additionally be found in the csv.</p> <p>Nomenclature</p> <p>CAMXXXXXX : unit ID corresponding to individual samples<br> _v _d: ventral or dorsal<br> </p> <p>Information on individual samples from the Butterfly Genetics Group Collection can be found on the public database Earthcape (click <a href="https://heliconius.ecdb.io/#ViewID=ContentPage_DetailView&ObjectKey=843e8ec1-41a6-4706-9622-f643132da859&ObjectClassName=EarthCape.Module.Core.ContentPage&mode=View">here</a> for the database, and <a href="http://heliconius.zoo.cam.ac.uk/databases/earthcape-specimen-database/">here</a> for FAQ)</p> <p>Please contact Chris Jiggins (c.jiggins[at]zoo.cam.ac.uk) for requests.</p> <p> </p> <p>------------------------------------------------------</p> <p>ES:</p> <p>Este repositorio contiene fotografías tomadas en el Butterfly Genetics Group de la Universidad de Cambridge</p> <p>Este lote contiene la colección de especímenes silvestres de las Islas Cook (Nueva Zelanda) colectadas por Quentin Paynter. Las fotografías se tomaron en tres grupos, con zoom y condiciones lumínicas algo distintas.</p> <p>Nomenclatura</p> <p>CAMXXXXXX: ID de unidad correspondiente a muestras individuales<br> _v _d: ventral o dorsal<br> </p> <p>Puede encontrar información sobre muestras individuales de Butterfly Genetics Group Collection en la base de datos pública Earthcape (haga clic <a href="https://heliconius.ecdb.io/#ViewID=ContentPage_DetailView&ObjectKey=843e8ec1-41a6-4706-9622-f643132da859&ObjectClassName=EarthCape.Module.Core.ContentPage&mode=View">aquí</a> para la base de datos, y <a href="http://heliconius.zoo.cam.ac.uk/databases/earthcape-specimen-database/">aquí</a> para preguntas frecuentes)</p> <p>Por favor, póngase en contacto con Chris Jiggins (c.jiggins [arroba] zoo.cam.ac.uk) con sus preguntas o peticiones.</p>
Clustering of loci controlling species differences in male chemical bouquets of sympatric Heliconius butterflies
<p>The degree to which loci promoting reproductive isolation cluster in the genome – <i>i.e. </i>the genetic architecture of reproductive isolation - can influence the tempo and mode of speciation. Tight linkage between these loci can facilitate speciation in the face of gene flow. Pheromones play a role in reproductive isolation in many Lepidoptera species, and the role of endogenously-produced compounds as secondary metabolites decreases the likelihood of pleiotropy associated with many barrier loci. <i>Heliconius </i>butterflies use male sex pheromones to both court females (aphrodisiac wing pheromones) and ward off male courtship (male-transferred anti-aphrodisiac genital pheromones), and it is likely that these compounds play a role in reproductive isolation between <i>Heliconius </i>species. Using a set of backcross hybrids between <i>H. melpomene </i>and <i>H. cydno</i>, we investigated the genetic architecture of putative male pheromone compound production. We found a set of 40 significant quantitative trait loci (QTL) representing 33 potential pheromone compounds. QTL clustered significantly on two chromosomes, chromosome 8 for genital compounds and chromosome 20 for wing compounds, and chromosome 20 was enriched for potential pheromone biosynthesis genes. There was minimal overlap between pheromone QTL and known QTL for mate choice and color pattern. Nonetheless, we did detect linkage between a QTL for wing androconial area and <i>optix</i>, a color pattern locus known to play a role in reproductive isolation in these species. This tight clustering of putative pheromone loci might contribute to coincident reproductive isolating barriers, facilitating speciation despite ongoing gene flow.</p>
Balanced polymorphisms and their divergence in a Heliconius butterfly
<p>The evolution of mimicry in similarly defended prey is well described by Müllerian mimicry theory, which predicts the convergence of warning patterns in order to gain the most protection from predators. However, despite this prediction, we can find great diversity of color patterns amongst Müllerian mimics such as <i>Heliconius </i>butterflies in the neotropics. Furthermore, some species have evolved the ability to maintain multiple distinct warning patterns in single populations, a phenomenon known as polymorphic mimicry. The adaptive benefit of these polymorphisms is questionable since variation from the most common warning patterns is expected to be disadvantageous as novel signals are punished by predators naive to them. In this study we use artificial butterfly models throughout Central and South America to characterize the selective pressures maintaining polymorphic mimicry in <i>Heliconius doris.</i> Our results highlight the complexity of positive frequency-dependent selection, the principal selective pressure driving convergence amongst Müllerian mimics, and its impacts on interspecific variation of mimetic warning coloration. We further show how this selection regime can both limit and facilitate the diversification of mimetic traits.</p>
Parallel evolution of behaviour, physiology and life history associated with altitudinal shifts in forest type in Heliconius butterflies
<p class="MsoNormal"><span>Parallel evolution of morphological traits is widely reported, providing evidence for the role of local conditions in driving adaptive divergence. Comparatively, fewer studies have tested for parallelism in behaviour, and it is less clear to what extent heritable behavioural shifts contribute to adaptive divergence. We exploit repeated incipient speciation across altitudinal gradients to explore behaviour and physiology in <em>Heliconius </em>butterflies adapted to high-elevation. We performed common garden experiments with <em>H. chestertonii, </em>a high-altitude specialist from the Colombian Cordillera Occidental, and <em>H. erato venus</em>, a low-elevation proxy for the ancestral population, and compared our results to existing data for an equivalent Ecuadorian taxa-pair. Using broad-scale climatic data, we show that both pairs diverge across similar ecological gradients, confirmed using localised data loggers in the ranges of <em>H. chestertonii</em> and <em>H. e. venus</em>. We further show that <em>H. chestertonii </em>and <em>H. e. venus</em> have divergent activity patterns, attributable to different responses to microclimate, and life histories. Finally, we provide evidence for parallelism in these traits with <em>H. himera</em> and <em>H. e. cyrbia</em>. We propose that this is a result of selection associated with independent colonisations of high-altitude forests, emphasising the importance of heritable behavioural and physiological adaptations during population divergence and speciation.</span></p>
Dataset for: Plasticity and genetic effects contribute to different axes of neural divergence in a community of mimetic Heliconius butterflies
<p>Changes in ecological preference, often driven by spatial and temporal variation in resource distribution, can expose populations to environments with divergent information content. This can lead to adaptive changes in the degree to which individuals invest in sensory systems and downstream processes, to optimize behavioural performance in different contexts. At the same time, environmental conditions can produce plastic responses in nervous system development and maturation, providing an alternative route to integrating neural and ecological variation. Here, we explore how these two processes play out across a community of <em>Heliconius</em> butterflies. <em>Heliconius</em> communities exhibit multiple Mullerian mimicry rings, associated with habitat partitioning across environmental gradients. These environmental differences have previously been linked to heritable divergence in brain morphology in parapatric species pairs. They also exhibit a unique dietary adaptation, known as pollen feeding, that relies heavily on learning foraging routes, or trap-lines, between resources, which implies an important environmental influence on behavioural development. By comparing brain morphology across 133 wild-caught and insectary reared individuals from seven <em>Heliconius</em> species, we find strong evidence for interspecific variation in patterns of neural investment. These largely fall into two distinct patterns of variation; first, we find consistent patterns of divergence in the size of visual brain components across both wild and insectary reared individuals, suggesting genetically encoded divergence in the visual pathway. Second, we find interspecific differences in mushroom body size, a central component of learning and memory systems, but only among wild caught individuals. The lack of this effect in common-garden individuals suggests an extensive role for developmental plasticity in interspecific variation in the wild. Finally, we illustrate the impact of relatively small-scale spatial effects on mushroom body plasticity by performing experiments altering the cage size and structure experienced by individual <em>H. hecale</em>. Our data provide a comprehensive survey of community level variation in brain structure, and demonstrate that genetic effects and developmental plasticity contribute to different axes of interspecific neural variation.</p>
Data & R Code for "Enhanced long-term memory and increased mushroom body plasticity in Heliconius butterflies"
<p>This ZIP file contains the data and R code used to analyse it for the paper "Enhanced long-term memory and increased mushroom body plasticity in Heliconius butterflies". Behavioural and neuroanatomical data are in separate folders.</p>
Dataset for: Plasticity and genetic effects contribute to different axes of neural divergence in a community of mimetic Heliconius butterflies
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Quantifying visual acuity in Heliconius butterflies
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Movement, translocation and MRR data for Heliconius butterflies
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Data From: Exploitation of an ancestral pheromone biosynthetic pathway contributes to diversification in Heliconius butterflies
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Data from: Gene duplication and gene expression changes play a role in the evolution of candidate pollen feeding genes in Heliconius butterflies
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