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Thermobiological effects of temperature-induced color variations in Aglais urticae (Lepidoptera, Nymphalidae).

ABSTRACT: Coloration of animals is important for camouflage, for social behavior, or for physiological fitness. This study investigates the color variation in adults of Aglais urticae obtained on subjecting some pre-imaginal stages to different temperature conditions and their thermobiological consequences. To investigate the evolutionary-ecological interactions of temperature and pigmentation in butterflies, caterpillars, and pupae of the small tortoiseshell, Aglais urticae (Lepidoptera, Nymphalidae), larvae from Central Europe and Scandinavia were reared at temperatures between 7 and 34°C in the laboratory or in the field. After emergence, the intensity of pigmentation of the imagines and their increase in body temperature under defined full-spectrum light irradiation were quantified by image analysis and thermal imaging. At constant conditions, ambient rearing temperature and pigmentation intensity of imagines were negatively and linearly correlated in Central European butterflies, regardless of whether the pupal stage alone or, additionally, the last period of the larval stage was exposed to these conditions: low temperatures induced darker coloration and high temperatures led to lighter individuals. A thermal pulse of a few days alone at the beginning of pupal dormancy led to a similar, albeit weakened, effect. Caterpillars of the Scandinavian subspecies A. urticae polaris, whose pupal dormancy took place under Central European field conditions, developed into strongly pigmented imagines. The thermobiological relevance of more intense pigmentation was shown by significantly higher absorption of light, and thus stronger increased body temperature after 5 min of defined illumination, but this difference ceased after 15 min. Our results show that phenotypic plasticity in wing coloration is adaptive since temperature-induced developmental changes provide thermobiological benefit in adult butterflies. We propose that, in subpolar latitudes, darker coloration likely has a selection advantage favoring individuals with reaction norms gradually shifted to stronger pigmented phenotypes, possibly leading to the establishment of a pigmentation cline.

SUBMITTER: Markl G

PROVIDER: S-EPMC9188032 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Herbivorous insects and host plants have developed a close and complex relationship over a long period of co-evolution. Some plants provide nutrients for insects, but plants' secondary metabolites also influence their growth and development. Urtica cannabina roots and leaves are poisonous, yet Aglais urticae larvae feed on them, so we aimed to clarify the mechanism enabling this interaction. At present, studies on the detoxification mechanism of the A. urticae are rare. In our study, first, we used the A. urticae larval odor selection behavior bioassay and choice feeding preference assay to analyze the feeding preferences of A. urticae on its host plant, U. cannabina. Next, we used transcriptome sequencing to obtain the unigenes annotated and classified by various databases, such as KEGG and GO. In this study, we found that U. cannabina could attract A. urticae larvae to feed via scent, and the feeding preference assay confirmed that larvae preferred U. cannabina leaves over three other plants: Cirsium japonicum, Cannabis sativa, and Arctium lappa. The activity of detoxifying enzymes GST and CarE changed in larvae that had consumed U. cannabina. Furthermore, through transcriptomic sequencing analysis, 77,624 unigenes were assembled from raw reads. The numbers of differentially expressed genes were calculated using pairwise comparisons of all life stages; the expression of detoxification enzyme genes was substantially higher in larvae than in the pupal and adult stages. Finally, we identified and summarized 34 genes associated with detoxification enzymes, such as UDP-glucose 4-epimerase gene, 5 Glutathione S-transferase genes, 4 Carboxylesterase genes, 4 Cytochrome P450 genes, 10 ATP-binding cassette genes, 4 Superoxide dismutase, and Peroxidase. Moreover, we identified 28 genes associated with the development of A. urticae. The qRT-PCR results were nearly consistent with the transcriptomic data, showing an increased expression level of four genes in larvae. Taken together, this study examines the correlation between A. urticae and host plants U. cannabina, uncovering a pronounced preference for A. urticae larvae toward host plants. Consistent with RNA-seq, we investigated the mechanism of A. urticae's interaction with host plants and identified detoxification-related genes. The present study provides theoretical support for studying insect adaptation mechanisms and biological control.

Project description:BackgroundMitogenomic phylogenies have revealed well-supported relationships for many eukaryote groups. In the order Lepidoptera, 113 species mitogenomes had been sequenced (May 14, 2014). However, these data are restricted to ten of the forty-three recognised superfamilies, while it has been challenging to recover large numbers of mitogenomes due to the time and cost required for primer design and sequencing. Nuclear rather than mitochondrial genes have been preferred to reconstruct deep-level lepidopteran phylogenies, without seriously evaluating the potential of entire mitogenomes. Next-generation sequencing methods remove these limitations by providing efficiently massive amounts of sequence data. In the present study, we simultaneously obtained a large number of nymphalid butterfly mitogenomes to evaluate the utility of mitogenomic phylogenies by comparing reconstructions to the now quite well established phylogeny of Nymphalidae.ResultsWe newly obtained 30 nymphalid mitogenomes via pyrosequencing on the Roche 454 GS Junior system, and combined these sequences with publicly accessible data to provide a 70-taxa dataset covering 37 genes for a 15,495 bp alignment. Polymorphic sites were not homogeneously distributed across the gene. Two gene regions, nad6 and 3' end of nad5, were most variable, whereas the cox1 and 5' ends of rrnL were most conserved. Phylogenetic relationships inferred by two likelihood methods were congruent and strongly supported (>0.95 posterior probability; ML bootstrap >85%), across the majority of nodes for multiple partitioning strategies and substitution models. Bayes factor results showed that the most highly partitioned dataset is the preferred strategy among different partitioning schemes. The most striking phylogenetic findings were that the subfamily Danainae not Libytheinae was sister of the remaining brush-footed butterflies and that, within Limenitidini, the genus Athyma was clearly polyphyletic. None of the single-gene phylogenies recovered the highly supported topologies generated on the basis of the whole mitogenomic data.ConclusionsThirty mitogenomes were assembled with 89% completeness from the contigs of pyrosequencing-derived reads. Entire mitogenomes or higher-quality sequences could be obtained by increasing pyrosequencing read coverage or by additional Sanger sequencing. Our mitogenomic phylogenies provide robust nodal support at a range of levels, demonstrating that mitogenomes are both accurate and efficient molecular markers for inferring butterfly phylogeny.

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Thermobiological effects of temperature-induced color variations in Aglais urticae (Lepidoptera, Nymphalidae).

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