High-Quality Genome Assembly and Comprehensive Transcriptome of the Painted Lady Butterfly Vanessa cardui.
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ABSTRACT:
SUBMITTER: Zhang L
PROVIDER: S-EPMC8290113 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Butterfly wing color patterns are an important model system for understanding the evolution and development of morphological diversity and animal pigmentation. Wing color patterns develop from a complex network composed of highly conserved patterning genes and pigmentation pathways. Patterning genes are involved in regulating pigment synthesis however the temporal expression dynamics of these interacting networks is poorly understood. Here, we employ next generation sequencing to examine expression patterns of the gene network underlying wing development in the nymphalid butterfly, Vanessa cardui.We identified 9, 376 differentially expressed transcripts during wing color pattern development, including genes involved in patterning, pigmentation and gene regulation. Differential expression of these genes was highest at the pre-ommochrome stage compared to early pupal and late melanin stages. Overall, an increasing number of genes were down-regulated during the progression of wing development. We observed dynamic expression patterns of a large number of pigment genes from the ommochrome, melanin and also pteridine pathways, including contrasting patterns of expression for paralogs of the yellow gene family. Surprisingly, many patterning genes previously associated with butterfly pattern elements were not significantly up-regulated at any time during pupation, although many other transcription factors were differentially expressed. Several genes involved in Notch signaling were significantly up-regulated during the pre-ommochrome stage including slow border cells, bunched and pebbles; the function of these genes in the development of butterfly wings is currently unknown. Many genes involved in ecdysone signaling were also significantly up-regulated during early pupal and late melanin stages and exhibited opposing patterns of expression relative to the ecdysone receptor. Finally, a comparison across four butterfly transcriptomes revealed 28 transcripts common to all four species that have no known homologs in other metazoans.This study provides a comprehensive list of differentially expressed transcripts during wing development, revealing potential candidate genes that may be involved in regulating butterfly wing patterns. Some differentially expressed genes have no known homologs possibly representing genes unique to butterflies. Results from this study also indicate that development of nymphalid wing patterns may arise not only from melanin and ommochrome pigments but also the pteridine pigment pathway.
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Project description:Butterfly eyespots are complex morphological traits that can vary in size, shape and color composition even on the same wing surface. Homology among eyespots suggests they share a common developmental basis and function as an integrated unit in response to selection. Despite strong evidence of genetic integration, eyespots can also exhibit modularity or plasticity, indicating an underlying flexibility in pattern development. The extent to which particular eyespots or eyespot color elements exhibit modularity or integration is poorly understood, particularly following exposure to novel conditions. We used perturbation experiments to explore phenotypic correlations among different eyespots and their color elements on the ventral hindwing of V. cardui. Specifically, we identified which eyespots and eyespot features are most sensitive to perturbation by heat shock and injection of heparin-a cold shock mimic. For both treatments, the two central eyespots (3 + 4) were most affected by the experimental perturbations, whereas the outer eyespot border was more resistant to modification than the interior color elements. Overall, the individual color elements displayed a similar response to heat shock across all eyespots, but varied in their response to each other. Graphical modeling also revealed that although eyespots differ morphologically, regulation of eyespot size and colored elements appear to be largely integrated across the wing. Patterns of integration, however, were disrupted following heat shock, revealing that the strength of integration varies across the wing and is strongest between the two central eyespots. These findings support previous observations that document coupling between eyespots 3 + 4 in other nymphalid butterflies.
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Project description:The extent of aerial flows of insects circulating around the planet and their impact on ecosystems and biogeography remain enigmatic because of methodological challenges. Here we report a transatlantic crossing by Vanessa cardui butterflies spanning at least 4200 km, from West Africa to South America (French Guiana) and lasting between 5 and 8 days. Even more, we infer a likely natal origin for these individuals in Western Europe, and the journey Europe-Africa-South America could expand to 7000 km or more. This discovery was possible through an integrative approach, including coastal field surveys, wind trajectory modelling, genomics, pollen metabarcoding, ecological niche modelling, and multi-isotope geolocation of natal origins. The overall journey, which was energetically feasible only if assisted by winds, is among the longest documented for individual insects, and potentially the first verified transatlantic crossing. Our findings suggest that we may be underestimating transoceanic dispersal in insects and highlight the importance of aerial highways connecting continents by trade winds.
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Project description:During metamorphosis, the wings of a butterfly sprout hundreds of thousands of scales with intricate microstructures and nano-structures that determine the wings' optical appearance, wetting characteristics, thermodynamic properties, and aerodynamic behavior. Although the functional characteristics of scales are well known and prove desirable in various applications, the dynamic processes and temporal coordination required to sculpt the scales' many structural features remain poorly understood. Current knowledge of scale growth is primarily gained from ex vivo studies of fixed scale cells at discrete time points; to fully understand scale formation, it is critical to characterize the time-dependent morphological changes throughout their development. Here, we report the continuous, in vivo, label-free imaging of growing scale cells of Vanessa cardui using speckle-correlation reflection phase microscopy. By capturing time-resolved volumetric tissue data together with nanoscale surface height information, we establish a morphological timeline of wing scale formation and gain quantitative insights into the underlying processes involved in scale cell patterning and growth. We identify early differences in the patterning of cover and ground scales on the young wing and quantify geometrical parameters of growing scale features, which suggest that surface growth is critical to structure formation. Our quantitative, time-resolved in vivo imaging of butterfly scale development provides the foundation for decoding the processes and biomechanical principles involved in the formation of functional structures in biological materials.
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Project description:BackgroundAnts with complex societies have fascinated scientists for centuries. Comparative genomic and transcriptomic analyses across ant species and castes have revealed important insights into the molecular mechanisms underlying ant caste differentiation. However, most current ant genomes and transcriptomes are highly fragmented and incomplete, which hinders our understanding of the molecular basis for complex ant societies.FindingsBy hybridizing Illumina, Pacific Biosciences, and Hi-C sequencing technologies, we de novo assembled a chromosome-level genome for Monomorium pharaonis, with a scaffold N50 of 27.2 Mb. Our new assembly provides better resolution for the discovery of genome rearrangement events at the chromosome level. Analysis of full-length isoform sequencing (ISO-seq) suggested that ?15 Gb of ISO-seq data were sufficient to cover most expressed genes, but the number of transcript isoforms steadily increased with sequencing data coverage. Our high-depth ISO-seq data greatly improved the quality of gene annotation and enabled the accurate detection of alternative splicing isoforms in different castes of M. pharaonis. Comparative transcriptome analysis across castes based on the ISO-seq data revealed an unprecedented number of transcript isoforms, including many caste-specific isoforms. We also identified a number of conserved long non-coding RNAs that evolved specifically in ant lineages and several that were conserved across insect lineages.ConclusionsWe produced a high-quality chromosome-level genome for M. pharaonis, which significantly improved previous short-read assemblies. Together with full-length transcriptomes for all castes, we generated a highly accurate annotation for this ant species. These long-read sequencing results provide a useful resource for future functional studies on the genetic mechanisms underlying the evolution of social behaviors and organization in ants.
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