Novel Sex-Specific Genes and Diverse Interspecific Expression in the Antennal Transcriptomes of Ithomiine Butterflies.

Publisher: Oxford University Press Country of Publication: England NLM ID: 101509707 Publication Model: Print Cited Medium: Internet ISSN: 1759-6653 (Electronic) Linking ISSN: 17596653 NLM ISO Abbreviation: Genome Biol Evol Subsets: MEDLINE

Original Publication: Oxford, UK : Oxford University Press

Butterflies*/genetics ; Arthropod Antennae*/metabolism ; Transcriptome*; Animals ; Female ; Male ; Sex Characteristics ; Receptors, Odorant/genetics ; Evolution, Molecular

The olfactory sense is crucial for organisms, facilitating environmental recognition and interindividual communication. Ithomiini butterflies exemplify this importance not only because they rely strongly on olfactory cues for both inter- and intra-sexual behaviors, but also because they show convergent evolution of specialized structures within the antennal lobe, called macroglomerular complexes (MGCs). These structures, widely absent in butterflies, are present in moths where they enable heightened sensitivity to, and integration of, information from various types of pheromones. In this study, we investigate chemosensory evolution across six Ithomiini species and identify possible links between expression profiles and neuroanatomical. To enable this, we sequenced four new high-quality genome assemblies and six sex-specific antennal transcriptomes for three of these species with different MGC morphologies. With extensive genomic analyses, we found that the expression of antennal transcriptomes across species exhibit profound divergence, and identified highly expressed ORs, which we hypothesize may be associated to MGCs, as highly expressed ORs are absent in Methona, an Ithomiini lineage which also lacks MGCs. More broadly, we show how antennal sexual dimorphism is prevalent in both chemosensory genes and non-chemosensory genes, with possible relevance for behavior. As an example, we show how lipid-related genes exhibit consistent sexual dimorphism, potentially linked to lipid transport or host selection. In this study, we investigate the antennal chemosensory adaptations, suggesting a link between genetic diversity, ecological specialization, and sensory perception with the convergent evolution of MCGs. Insights into chemosensory gene evolution, expression patterns, and potential functional implications enhance our knowledge of sensory adaptations and sexual dimorphisms in butterflies, laying the foundation for future investigations into the genetic drivers of insect behavior, adaptation, and speciation.
Competing Interests: Conflict of Interest The authors declare no conflicts of interest.
(© The Author(s) 2024. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.)

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Keywords: antennal transcriptomics; chemosensory genes; comparative genomics; sensory adaptation; sexual dimorphism

0 (Receptors, Odorant)

Date Created: 20241007 Date Completed: 20241024 Latest Revision: 20241113

20241113

PMC11500719

10.1093/gbe/evae218

39373182