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Evolutionary conservation of opsin gene expression patterns in the compound eyes of darkling beetles

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Abstract

Recent large-scale studies of opsin gene contents in representatives of the largest order of insects, the Coleoptera (beetles), revealed that the blue wavelength-sensitive (B) opsin subfamily is absent in this clade, while the ultraviolet- (UV) and long wavelength-sensitive (LW) opsin subfamilies are broadly conserved with gene duplications possibly reintroducing blue sensitivity in select subclades. Little is known yet, however, how opsin genes are expressed in the compound eyes of beetles. In a previous study, we analyzed opsin gene expression in the red flour beetle Tribolium castaneum, a member of the family of darkling beetles (Tenebrionidae), and found that a singleton LW opsin homolog is homogeneously expressed in all photoreceptors of the compound eye retina with a singleton UV opsin homolog being co-expressed in the R7 subtype photoreceptors. To probe for the evolutionary conservation of these expression patterns, we isolated complete opsin transcript sequences from three additional species in the subfamily Tenebrionidae (Tribolium confusum, Tenebrio molitor, Zophobas morio) and studied their expression via whole mount in situ hybridization in the pupal retina. These experiments revealed very similar, if not identical, photoreceptor subtype-specific expression patterns in all three species compared with T. castaneum. Documenting a deep conservation of photoreceptor subtype-specific opsin gene expression in this range of darkling beetles, our study provides a first point of reference for broader comparative studies of retinal organization in the Coleoptera.

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Acknowledgments

We thank Sue Brown and Michael Wade for providing T. confusum and Camilla Sharkey and the three anonymous reviewers for their helpful comments on the manuscript.

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Authors and Affiliations

  1. Department of Immunology, Harvard Medical School, Boston, MA, USA

    Meng Wu

  2. Hillman Cancer Center, University of Pittsburgh Medical Center, Pittsburgh, PA, USA

    Riyue Bao

  3. Department of Medicine, University of Pittsburgh, Pittsburgh, PA, USA

    Riyue Bao

  4. Department of Biological Sciences, Wayne State University, 5047 Gullen Mall, Detroit, MI, 48202, USA

    Markus Friedrich

  5. Department of Anatomy and Cell Biology, Wayne State School of Medicine, Detroit, MI, USA

    Markus Friedrich

Authors
  1. Meng Wu
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  2. Riyue Bao
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  3. Markus Friedrich
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Correspondence to Markus Friedrich.

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Communicated by Nico Posnien

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Electronic supplementary material

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ESM 4

Multiple protein sequence alignments of UV- and LW opsin homologs (PPTX 66 kb)

ESM 5

Maximum likelihood gene tree analysis of the newly isolated tenebrionid UV- and LW opsin homologs. Numbers at branches indicate non-parametric bootstrap branch support values. Species abbreviations: Amel = Apis mellifera, Tcas = T. castaneum, Tcon = T. confusum, Tmol = T. molitor, Zmor = Z. morio. Scale bar corresponds to 0.1 substitutions per site. (DOCX 12 kb)

ESM 6

Comparison of body lengths, thorax widths, and eye sizes (XLSX 5 kb)

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Wu, M., Bao, R. & Friedrich, M. Evolutionary conservation of opsin gene expression patterns in the compound eyes of darkling beetles. Dev Genes Evol 230, 339–345 (2020). https://doi.org/10.1007/s00427-020-00669-2

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