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Jiggins, C. D.

Publications and source records attributed to Jiggins, C. D..

At least 19 recordsLinked to original sources

A shared molecular target hides distinct genetic routes to diamide resistance in Helicoverpa armigera (Lepidoptera: Noctuidae)

Diamide insecticides target insect ryanodine receptors (RyRs) and are widely used against lepidopteran pests, yet it remains unclear whether compounds sharing this molecular target evolve resistance through the same genetic routes. Here, we integrated RyR sequencing, structural modelling and population genomics to investigate resistance to chlorantraniliprole and flubendiamide in the global agricultural pest Helicoverpa armigera. We identified G4946E together with F4947I, a previously undescribed resistance-associated RyR substitution, in a chlorantraniliprole-resistant strain. Structural modelling indicated that F4947I may modify G4946E's effects on the diamide-binding pocket, while field and population-genomic evidence independently implicated the RyR-containing chromosome 28 region in chlorantraniliprole resistance. By contrast, high-level flubendiamide resistance occurred without amino acid substitutions in the RyR region examined, and field survival was predominantly associated with chromosome 2, independently recapitulating a previously identified resistance locus. Together, our findings reveal that resistance to insecticides sharing the same molecular target can evolve through distinct but potentially overlapping genetic routes, highlighting the limitations of predicting cross-resistance from target-site variation alone and the need for broader genomic approaches to resistance surveillance.

molecular biology↗

Adaptation in the eye and brain contributes to species divergence in visual perception in Heliconius butterflies

Sensory systems mediate the interaction between organisms and their environment, but how complex sensory pathways evolve and relate to variation in perception and behavior across ecological contexts, remains poorly understood, especially for terrestrial taxa. Here, we investigate whole-visual-system adaptation in Heliconius erato butterflies. Using continent-wide sampling, we demonstrate that within H. erato, facet count significantly decreased with increasing elevation. Common-garden rearing of low-elevation H. erato populations from Ecuador and their high-elevation sister species, H. himera, showed that eye and brain morphology are heritable, and comparisons to genomic measures of divergence indicates that this variation is due to divergent selection. Parallel comparisons from Colombia involving H. chestertonii (high elevation) and H. erato venus (low elevation) further revealed that eye and brain morphology can evolve as independent, decoupled traits. For both locations, differences in visual acuity correlated with variation in facet count. We also observed parallel evolution of spectral sensitivity, with independent high-elevation populations having fewer red-reflecting lateral filtering pigments. To experimentally link visual system morphology to behavior, we assessed visual acuity in second-generation H. erato cyrbia-H. himera hybrids. Overall, acuity was influenced by facet count, and when analyzed together with brain morphology, by a positive interaction between facet count and optic lobe volume, demonstrating that structural investment in the eye and neural expansion combine to maximize visual perception. This work shows that visual adaptation is a multi-layered process whereby sensory traits can evolve independently under localized ecological pressures, but evolution across the visual pathway contributes to refinements in behavioral performance.

evolutionary biology↗

Genetically informed distribution models refine predictions for the overwintering range of Helicoverpa armigera in North America

The ecological and economic threat posed by invasive pests demands proactive mitigation. Species distribution models (SDMs) are widely used in efforts to predict where invasive species might spread after introduction, though such models face several limitations. Among these is the unrealistic assumption of niche uniformity throughout a species' range. This has led to interest in developing SDMs that explicitly account for local adaptation, though few methods have achieved this in a way that confidently separates local adaptation from population structure. Here we develop and implement a sequential SDM approach that incorporates experimentally verified associations between genotype, phenotype, and environment to forecast establishment risk in a major agricultural pest. We leverage genomic data from 738 individuals to characterize the geographic distribution of alleles at a major-effect locus for cold tolerance (tret1) in Helicoverpa armigera, an invasive crop pest of major economic concern in North America. We demonstrate that a recently detected North American population carries a cold-adapted tret1 allele, which has likely contributed to its persistence. We quantify the contribution of cold-adapted tret1 to the potential invasive range of H. armigera in North America under current and future climate scenarios. We find that cold-adapted tret1 may dramatically expand the potential range of H. armigera, and that potential future range expansion is likely to be driven primarily by cold-adapted individuals. Our results highlight the importance of accounting for intraspecific variation in invasive species risk assessments and management strategies.

ecology↗

Independent major-effect loci and limited trait associations characterise warning colour variation across sexes and life stages in the wood tiger moth (Arctia plantaginis)

Variation in warning colouration is common, despite strong positive frequency-dependent selection favouring the most common morph, and may arise from spatially or temporally variable selection or associations with other traits. We investigated the maintenance of warning colour variation in the wood tiger moth, Arctia plantaginis, which shows sexual dimorphism in colouration: two distinct male morphs controlled by a single locus, and continuous variation in female hindwing colour and larval warning signal size. Using whole-genome sequencing of 657 individuals from a laboratory stock derived from a wild polymorphic population, we examined the genetic basis of multiple life-history traits, chemical defence, pheromones, and male activity. We specifically tested for associations with male colour and aimed to identify the genetic basis of female and larval colour variation. We detected separate major-effect loci for female colour and larval signal size, which were different from the male colour locus. Hindwing melanism was the only trait associated with male colour, mapping to a nearby major-effect locus and showing a link to reduced activity at higher temperatures. Female colour was phenotypically correlated with pheromone amount. However, apart from melanism, none of the other traits measured showed an association with any of the loci controlling warning colours and we found no evidence that male colour is part of a supergene or complex co-adapted phenotype. Instead, our results indicate largely independent genetic architectures for warning colours suggesting that variable selection rather than genetic associations may contribute to the maintenance of colour polymorphisms in this species.

evolutionary biology↗

The collision of two genomes threatens global food security

Human activity alters selection pressures and redistributes biodiversity, creating opportunities for hybridization when dilerent species come into secondary contact. It is now well-established that ancient hybridization plays an important role in adaptive radiation 1, but its role in recent anthropogenic adaptation remains unclear. We investigated this in a study of hybridizing native and invasive Helicoverpa moths in Brazil, which are among the most economically damaging crop pests globally. Native H. zea has recently evolved Bt resistance and is better adapted to maize as a host plant, while invasive H. armigera is resistant to pyrethroid pesticides and is better adapted to soybean. Using a decade-long time series of 975 genomes from both species, we demonstrate rapid, bidirectional adaptive introgression of structural variants that cause resistance to two distinct pesticides. In one direction, a pyrethroid resistance gene from H. armigera (CYP337B3) is now almost fixed in native H. zea. In the other direction, ~30% of recently-sampled invasive H. armigera carry a H. zea-derived trypsin repeat cluster. Using controlled crosses, we show that this trypsin repeat cluster confers resistance to Bt (Cry1Ac) soy in the H. armigera genomic background. Thus, hybridization has combined H. armigera adaptation to soy with H. zea Cry1Ac resistance to facilitate exploitation of Brazilian Bt soy monoculture -- a vast anthropogenic habitat exceeding the area of Germany. Our results show that the combinatorial mechanisms that produce biodiversity can also drive rapid anthropogenic adaptation on ecological timescales, with consequences for global food security.

evolutionary biology↗

Disentangling local adaptation and phenotypic plasticity in traits associated with altitude and temperature in widespread tropical butterflies

Climatic stratifications, in particular differences in temperature, occur along altitudinal clines. Understanding genetic and phenotypic divergence across these regions can give insight into speciation and diversification, as well as aid in our knowledge of how species may respond to possible climate change scenarios. Most past research has focused on temperate regions, yet it is in the tropics that organisms are thought to be the most vulnerable to rising temperatures. In addition, year-round stable temperatures in the tropics make altitudinal temperature variation more pronounced and increase the likelihood of local adaptation across relatively narrow gradients. Here we investigate how genetics and the environment influence a wide range of traits in two butterfly species, Heliconius erato and Heliconius melpomene, which are widespread across the neotropics and occur along the altitudinal slope of the Andes. Using common garden rearing of over 1,000 offspring from over 70 wild females caught along an altitudinal gradient, as well as rearing of populations from either end of the altitudinal range in their reciprocal temperature environments, we find evidence of genetic, environmental, and in some cases gene-by-environment interaction effects in developmental, morphological, and thermal tolerance traits. We find parallel divergence in wing colour in both species, with wing colour darkening with increasing altitude, consistent with this playing a role in thermoregulation in these species where wing colour has mostly been linked to mimicry and mate choice. We also find evidence for gene-by-environment interactions: In H. erato we found local differences in heat acclimation response, with increased heat knock-out times at higher rearing temperatures found only in low altitude populations, which are exposed to the hottest temperatures. We find evidence for heritable genetic variation in most traits measured, with positive implications for adaptation to climate change, although our results suggest that selection may not act in a straightforward way on these traits.

ecology↗

Gene loss associated with plasticity-first evolution in Heliconius butterflies

Phenotypic plasticity occurs when a genotype can produce more than one phenotype under different environmental conditions. Genetic accommodation allows plastic phenotypes to be tuned to new environments and eventually to even be lost. The colourful and toxic Heliconiini butterflies have biochemical plasticity - they either sequester their cyanogenic glucosides (CG) from their larval hostplant or biosynthesize them when compounds for sequestration are not available. Here, we trace the evolution of CG biosynthesis in Heliconiini butterflies, a fundamental component of this biochemical plasticity. We first reconstructed the evolutionary history of biochemical plasticity in Heliconiini butterflies using chemical data from over 700 individuals, demonstrating that plasticity was ancestral in the tribe and further lost in a few clades, such as the Sapho clade that only sequester CGs. In lepidopterans, CG biosynthesis has been fully characterized in the moth Zygaena filipendulae, and is composed of CYP405A2, CYP332A3, and UGT33A1. Thus, we CRISPR-edited the gene CYP405 in Heliconius erato, and confirmed that CYP405-knockout caterpillars do not biosynthesize CGs. We identified the CYP405s and CYP332s in other lepidopterans and found that both genes were independently co-opted into CG biosynthesis in the Heliconiinae butterflies and Zygaena moths. Most lepidopterans have a CYP332, but CYP405 is mostly restricted to butterflies and has been duplicated in all Heliconius species. Although several CYP405 copies were found in the Sapho clade, they lack structurally important P450 domains, which explain they loss of biochemical plasticity via specialization in CG sequestration. Our findings represent one of the few examples of plasticity-first evolution in which the genetic mechanisms associated with its accommodation/assimilation are known.

evolutionary biology↗

Functional analysis of gene family evolution demonstrates expansion of digestive, immunity and olfactory functions in the black soldier fly (Hermetia illucens) lineage

Structural variants such as chromosomal rearrangements and gene duplications can play an important role in the adaptation and diversification of organisms. Here, we used comparative genomics to study the functional implications of structural variants across two families of flies. We compared the reference genomes of eight Asilidae species and six Stratiomyidae species, including the black soldier fly (Hermetia illucens), a species with an ability to convert organic waste into biomass and a recently expanded global range. The genomes of Stratiomyidae are generally larger than Asilidae and contain a higher proportion of transposable elements, many of which are recently expanded. Gene families showing more gene duplications are enriched for life history related functions such as metabolism in Stratiomyidae and proteolysis and longevity in Asilidae. Gene families showing more gene duplications that are specific to H. illucens are mostly related to olfactory and immune responses, while across the Stratiomyidae there is enrichment of digestive and metabolic functions such as proteolysis. Together, our results shed light on gene family expansions that have likely played a role in the ecological success of the black soldier fly.

genomics↗

Caterpillar counter-adaptations to hooked trichomes: does the coevolutionary arms race continue?

Plants protect themselves against herbivory with diverse chemical and physical defences, and many herbivores have evolved counter-adaptations against these defences. So far, little is known about herbivore counter-adaptations to physical plant defences and their underlying mechanisms. Here, we investigated how specialised Heliconiini caterpillars are able to cope with the hooked trichomes of Passiflora adenopoda vines. P. adenopoda trichomes have sharp tips reinforced with silica, in contrast to simpler trichomes of other Passiflora that do not deter Heliconiini larvae. While Heliconius melpomene and H. erato caterpillars placed on P. adenopoda leaves were arrested and their soft cuticle was pierced by the sharp hooked trichomes, H. charithonia and Dryas iulia caterpillars of all sizes could move easily over the leaves without any injury. The superior performance of these two species on trichome-bearing leaves can be explained by their thicker and more puncture-resistant cuticle. Morphological and penetrometry measurements showed that the relevant cuticle regions in H. charithonia and D. iulia caterpillars are significantly thicker and more puncture-resistant than in H. melpomene and H. erato. When we tested the ability of the caterpillars to feed on P. adenopoda leaves with hooked trichomes, only H. charithonia survived, indicating the existence of further, previously unknown post-ingestive adaptations. Understanding insect counter-adaptations to physical plant defences is essential for studying the evolutionary arms-race between plants and insect herbivores.

evolutionary biology↗

Repeatable phenotypic but not genetic response to selection on body size in the black soldier fly

Polygenic traits are expected to show high genetic redundancy and therefore low repeatability in the genomic response to selection. We tested this prediction by selecting for large body size in the black soldier fly (Hermetia illucens). Over three replicate experiments selected for large body size, we found a strong and repeatable phenotypic response, with a mean 15% increase in body size. Selected lines also increased in larval growth rate (+19%) and average protein content (+14%), suggesting that selection on large body size does not result in strong trade-offs. In contrast to the predictability of the phenotypic response across replicates, whole genome sequencing identified a highly polygenic and non-repeatable genomic response. We identified 120, 301 and 157 outlier genomic regions in the three replicates, but high redundancy with only four shared regions. Among 12 candidate genes found in these regions, the insulin-like receptor gene (HiInR) was confirmed as regulating larval growth using a CRISPR knockout experiment. In summary, polygenic quantitative traits show high genetic redundancy, even where the phenotypic response to selection is highly repeatable.

evolutionary biology↗

The genetic architecture of resistance to flubendiamide insecticides in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae)

Insecticide resistance is a major problem in food production, environmental sustainability, and human health. The cotton bollworm Helicoverpa armigera is a globally distributed crop pest affecting over 300 crop species. H. armigera has rapidly evolved insecticide resistance, making it one of the most damaging pests worldwide. Understanding the genetic basis of insecticide resistance provides insights to develop tools, such as molecular markers, that can be used to slow or prevent the evolution of resistance. We explore the genetic architecture of H. armigera resistance to a widely used insecticide, flubendiamide, using two complementary approaches: genome-wide association studies (GWAS) in wild-caught samples and quantitative trait locus (QTL) mapping in a controlled cross of susceptible and resistant laboratory strains. Both approaches identified one locus on chromosome 2, revealing two SNPs within 976 bp that can be used to monitor field resistance to flubendiamide. This was the only region identified using linkage mapping, though GWAS revealed additional sites associated with resistance. Other loci identified by GWAS in field populations contained known insecticide detoxification genes from the ATP-binding cassette family, ABCA1, ABCA3, ABCF2 and MDR1. Our findings revealed an oligogenic genetic architecture, in contrast to previous reports of monogenic resistance associated with the ryanodine receptor. This work elucidates the genetic basis of rapidly evolving insecticide resistance and will contribute to the development of effective insecticide resistance management strategies. Author summaryInsecticide resistance in agricultural pests challenges food security, environmental sustainability, and human health. The cotton bollworm Helicoverpa armigera is resistant to various insecticide classes as well as Bacillus thuringiensis toxins. Understanding the genetic basis of this resistance is crucial for developing effective insecticide resistance management (IRM) strategies. Our study investigated the genetic architecture of resistance of H. armigera to flubendiamide and identified SNPs associated with resistance. We used two approaches: association mapping in wild-derived samples and QTL mapping in a controlled backcross of susceptible and resistant laboratory strains. One specific region on chromosome 2 was found in both GWAS and QTL mapping analysis and showed significant potential as a PCR-based marker for monitoring resistance to flubendiamide in H. armigera. Additionally, the GWAS identified five more SNPs in the field populations. The candidate genes identified are primarily associated with insecticide detoxification mechanisms and calcium homeostasis. Our study advances the understanding of the complex genetic architecture of flubendiamide resistance in H. armigera, providing valuable tools for IRM programs and establishing a basis for future studies.

genetics↗

Genomics of Neotropical biodiversity indicators: two butterfly radiations with rampant chromosomal rearrangements and hybridisation

A major question in evolutionary biology is what drives the diversification of lineages. Rapid, recent radiations are ideal systems for addressing how new species arise because they still show key morphological and ecological adaptations associated with speciation. While most studied recent radiations have evolved in an insular environment, less research has been carried out on continental radiations with complex species interactions. Melinaea and Mechanitis butterflies (Nymphalidae: Ithomiini) have rapidly radiated in the Neotropics. They are classical models for Amazonian biogeography and colour pattern mimicry and have been proposed as biodiversity indicators. We generated reference genomes for five species of each genus, and whole-genome resequencing data of most species and subspecies covering a wide geographic range to assess phylogeographic relationships, patterns of hybridisation and chromosomal rearrangements. Our data help resolve the classification of these taxonomically challenging butterflies and reveal very high diversification rates. We find rampant evidence of historical hybridisation and putative hybrid species in both radiations, which may have facilitated their rapid diversification. Moreover, dozens of chromosomal fusions and fissions were identified between congeneric species, and even some within species. We conclude that interactions between geography, hybridisation and chromosomal rearrangements have contributed to these two rapid radiations in the highly diverse Neotropical region. We suggest that rapid radiations may be spurred by repeated periods of geographic isolation during Pleistocene climate oscillations, combined with lineage-specific rapid accumulation of incompatibilities during allopatric phases, followed by secondary contact with some gene exchange. Significance StatementUnderstanding factors contributing to rapid speciation is a key aim of evolutionary biology. Here we focus on two rapid radiations of Neotropical butterflies. Our genomic data with broad taxonomic and geographic coverage reveal rampant hybridisation and chromosomal rearrangements, each likely contributing to the high diversification rates. Our study highlights the use of genomic data to resolve taxonomically challenging species groups and elucidate drivers of diversification in rapid radiations. We show that for biodiversity hotspots with recent radiations, barcoding is insufficient to characterise species richness due to gene flow and recent speciation. The taxonomic implications of both introgression and karyotype diversity for species delimitation are important to consider during monitoring and management of biodiversity in these vulnerable habitats.

evolutionary biology↗

A long non-coding RNA at the cortex locus controls adaptive colouration in butterflies

Evolutionary variation in the wing pigmentation of butterflies and moths offers striking examples of adaptation by crypsis and mimicry. The cortex locus has been independently mapped as the locus controlling colour polymorphisms in 14 lepidopteran species, suggesting it acts as a genomic hotspot for the diversification of wing patterns, but functional validation through protein-coding knockouts has proven difficult to obtain. Our study unveils the role of a novel long non-coding RNA (lncRNA) which we name ivory, transcribed from the cortex locus, in modulating colour patterning in butterflies. Strikingly, ivory expression prefigures most melanic patterns during pupal development, suggesting an early developmental role in specifying scale identity. To test this, we generated CRISPR mosaic knock-outs in five nymphalid butterfly species and show that ivory mutagenesis yields transformations of dark pigmented scales into white or light-coloured scales. Genotyping of Vanessa cardui germline mutants associates these phenotypes to small on-target deletions at the conserved first exon of ivory. In contrast, cortex germline mutant butterflies with confirmed null alleles lack any wing phenotype, and exclude a colour patterning role for this adjacent gene. Overall, these results show that a lncRNA acts as a master switch of colour pattern specification, and played key roles in the adaptive diversification of colour patterns in butterflies. Significance statementDeciphering the genetic underpinnings of adaptive variation is fundamental for a comprehensive understanding of evolutionary processes. Long non-coding RNAs (lncRNAs) represent an emerging category of genetic modulators within the genome, yet they have been overlooked as a source of phenotypic diversity. In this study, we unveil the pivotal role of a lncRNA in orchestrating colour transitions between dark and light patterns during butterfly wing development. Remarkably, this lncRNA gene is nested within the cortex locus, a genetic region known to control multiple cases of adaptive variation in butterflies and moths, including iconic examples of natural selection. These findings highlight the significant influence of lncRNAs in developmental regulation, and also underscore their potential as key genetic players in the evolutionary process itself.

evolutionary biology↗

Adaptive divergence in the eyes of Heliconius butterflies likely contributes to pre- and post mating isolation

When populations experience different sensory conditions, natural selection may favor whole sensory system divergence, from the peripheral structures to the brain. We characterized the outer eye morphology of sympatric Heliconius species from different forest types, and their first-generation reciprocal hybrids to test for adaptive visual system divergence and hybrid disruption. In Panama, Heliconius cydno occurs in closed forests, whereas Heliconius melpomene resides in more open areas. Previous work has shown that, among wild individuals, H. cydno has larger eyes than H. melpomene, and there are heritable, habitat-associated differences in the visual brain structures that exceed neutral divergence expectations. Notably, hybrids have intermediate neural phenotypes, suggesting disruption. To test for similar effects in the visual periphery, we reared both species and their hybrids in common garden conditions. We confirm that H. cydno has larger eyes and provide new evidence that this is driven by selection. Hybrid eye morphology is more H. melpomene-like despite body size being intermediate, contrasting with neural trait intermediacy. Thus, eye morphology differences between H. cydno and H. melpomene are consistent with adaptive divergence, and when combined with previous neuroanatomy data, suggest hybrid visual system disruption due to mismatched patterns of intermediacy and dominance in the visual pathway.

evolutionary biology↗

Cryptic diversity and signatures of domestication in the Black Soldier Fly (Hermetia illucens)

The Black Soldier Fly (Hermetia illucens) is the main species in the developing global industry of insects as food and feed, but little is known about its natural diversity or the genetic basis of its domestication. We obtained whole genome sequences for 54 individuals from both wild and captive populations. We identified two genetic lineages at least 3 million years divergent, revealing cryptic diversity within the species. Our study indicates that the most common populations used for commercial and academic applications are primarily derived from just one of these lineages, likely originating from a wild North American progenitor. We find that captive populations show strong reductions in genetic diversity, consistent with genome-wide effects of population bottlenecks and drift associated with rearing in captivity. Some limited evidence of gene flow between divergent lineages was observed, as well as evidence of hybridisation from domesticated populations into the wild. Our study suggests that natural genetic diversity could provide important variation for industrial purposes in this novel agricultural species. Author SummaryAnimals and plants have been domesticated by humans over thousands of years, shaping their genomes and yielding beneficial or improved traits for agriculture. Insect farming has recently reached industrial scales in order to recycle organic wastes into feed and food grade material. The Black Soldier Fly is the flagship insect species in this novel agriculture sector. However, the understanding of its evolutionary history and the genetic impact of intense farming has not been well studied to date. We examined whole genomes from populations sampled from across the worldwide distribution of Black Soldier Fly to investigate the impact of domestication and reveal the evolutionary history of the species. We found that farmed populations show distinct genomic regions showing reduced variation that could represent signatures of selection or demographic effects. We also identify two distinct lineages of Black Soldier Fly that have been diverging for millions of years, comparable to divergence between different species in other insect groups, yet show evidence of genetic exchange, indicating a lack of reproductive incompatibility in the populations tested. This work is the first to describe the genetic impact of domestication in the Black Soldier Fly and provide evolutionary insights using whole genomes. These results imply that considerable wild diversity could be harnessed for improving agricultural efficiency.

genomics↗

Rapid evolution of pesticide resistance via adaptation and interspecific introgression in a major North American crop pest

Insect crop pests threaten global food security. This threat is amplified through the spread of non-native species and the evolution of pesticide resistance, which can be introduced to a population though de novo mutation or gene flow. We investigate these processes in an economically important noctuid crop pest, Helicoverpa zea, which has rapidly evolved resistance to several pesticides. Its sister species Helicoverpa armigera, first detected as an invasive species in Brazil in 2013, introduced the pyrethroid resistance gene CYP337B3 to South American H. zea via introgression. To understand whether this contributes to pesticide resistance in North America, we sequenced 237 H. zea genomes across 10 sample sites in the US. First, we report H. armigera introgression into the North American H. zea population. Two individuals sampled in Texas in 2019 carry H. armigera haplotypes in a 4Mbp region containing CYP337B3. Second, we show that the remarkable dispersal ability of H. zea results in a panmictic North American population. Third, we detect signatures of selection in non-admixed H. zea, identifying a selective sweep at a second pesticide resistance locus with a similar name: CYP333B3. We estimate that its derived allele conferred a [~]4.9% fitness advantage and show that this estimate explains independently observed rare nonsynonymous CYP333B3 mutations approaching fixation over a [~]20-year period. We also detect putative signatures of selection at a kinesin gene associated with Bt resistance. Our results show that pesticide resistance in H. zea evolved rapidly and recently via two independent mechanisms: interspecific introgression and rapid intraspecific adaptation.

evolutionary biology↗

Transposable element insertions are associated with Batesian mimicry in the pantropical butterfly Hypolimnas misippus

Hypolimnas misippus is a Batesian mimic of the toxic African Queen butterfly (Danaus chrysippus). Female H. misippus butterflies use two major wing patterning loci (M and A) to imitate the four colour morphs of D. chrysippus found in different regions of Africa. In this study, we examine the evolution of the M locus and identify it as an example of adaptive atavism. This phenomenon involves a morphological reversion to an ancestral character that results in an adaptive phenotype. We show that H. misippus has re-evolved a wing pattern present in other Hypolimnas species for Batesian mimicry of a D. chrysippus morph. Using haplotagging, a linked-read sequencing technology, we discover two large transposable element (TE) insertions located at the M locus and establish that these insertions are present in the dominant allele responsible for producing the ancestral and mimetic phenotype. By conducting a comparative analysis involving additional Hypolimnas species, we demonstrate that the dominant allele is derived. This suggests that the TEs disrupt a cis-regulatory element, leading to the reversion to an ancestral phenotype that is then utilized for Batesian mimicry of a distinct model, a different morph of D. chrysippus. Our findings present a compelling instance of convergent evolution and adaptive atavism, in which the same pattern element has independently evolved multiple times in Hypolimnas butterflies, repeatedly playing a role in Batesian mimicry of diverse model species.

evolutionary biology↗

The Hypolimnas misippus genome supports a common origin of the W chromosome in Lepidoptera

Moths and butterflies (Lepidoptera) have a heterogametic sex chromosome system with females carrying ZW chromosomes and males ZZ. The lack of W chromosomes in early diverging lepidopteran lineages has led to the suggestion of an ancestral Z0 system in this clade and a B chromosome origin of the W. This contrasts with the canonical model of W chromosome evolution in which the W would have originated from the same homologous autosomal pair as the Z chromosome. Despite the distinct models proposed, the rapid evolution of the W chromosome has hindered the elucidation of its origin. Here, we present high-quality, chromosome-level genome assemblies of two Hypolimnas species (Hypolimnas missipus and Hypolimnas bolina) and use the H. misippus assembly to explore the evolution of W chromosomes in butterflies and moths. We show that in H. misippus the W chromosome has higher similarity to the Z chromosome than any other chromosome, which could suggest a possible origin from the same homologous autosome pair as the Z chromosome. However, using genome assemblies of closely related species (ditrysian lineages) containing assembled W chromosomes, we present contrasting evidence suggesting that the W chromosome might have evolved from a B chromosome instead. Crucially, by using a synteny analysis to infer homology, we show that W chromosomes are likely to share a common evolutionary origin in Lepidoptera. This study highlights the difficulty of studying the evolution of W chromosomes and contributes to better understanding its evolutionary origins. SignificanceButterflies and moths have a sex determination system in which females carry two different sex chromosomes, Z and W, while males carry two copies of the Z. The evolutionary origin of the W chromosome has been elusive, with many possible scenarios being suggested, such as the independent evolution of W chromosomes in many butterfly and moth species. Here, we present genome assemblies of two Hypolimnas butterfly species and use one of them to shed light on the evolution of the W chromosome. We show that W chromosomes across butterflies and moths are very similar which suggests a shared common origin.

genomics↗