Skip to main content
SpringerLink
Log in

A study of common scorpionfly (Mecoptera: Panorpidae) visual systems reveals the expression of a single opsin

  • Original Article
  • Published:
Organisms Diversity & Evolution Aims and scope Submit manuscript

Abstract

Knowledge of insect color vision and the genes that support color vision has been growing recently. Yet, research on some groups is limited (e.g., Mecoptera). Common scorpionflies (Panorpidae) are highly visual insects with many intriguing behaviors. We hypothesized that the family Panorpidae employs a complex color vision system and predicted that multiple opsin classes are expressed in the lineage. Transcriptomes were generated from the eye tissues for two species of Panorpidae (Panorpa acuminata and P. nebulosa) and one species of Boreidae (Boreus coloradensis). Opsins isolated from the transcriptomes were combined in a phylogenetic analysis with opsin sequences from other insect orders (e.g., those that are sensitive to ultraviolet, blue, and long wavelength light as part of the photopigment). A single long-wavelength opsin sequence was recovered from the panorpid species, while all three opsin classes (ultraviolet, blue, and long-wavelength) were recovered from the boreid. Among insects, this represents a potential case of monochromy due to a loss of opsin gene expression in the blue and ultraviolet portions of the visible light spectrum.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Arnold, K., Bordoli, L., Kopp, J., & Schwede, T. (2006). The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics, 22(2), 195–201.

    Article  CAS  PubMed  Google Scholar 

  • Beutel, R. G., Friedrich, F., & Whiting, M. F. (2008). Head morphology of Caurinus (Boreidae, Mecoptera) and its phylogenetic implications. Arthropod Structure & Development, 37(5), 418–433.

    Article  Google Scholar 

  • Biasini, M., Bienert, S., Waterhouse, A., Arnold, K., Studer, G., Schmidt, T., Kiefer, F., Cassarino, T. G., Bertoni, M., & Bordoli, L. (2014). SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Research. doi:10.1093/nar/gku340.

    PubMed  PubMed Central  Google Scholar 

  • Blankenberg, D., Kuster, G. V., Coraor, N. Ananda, G. Lazarus, R. Mangan, M. Nekrutenko A., & Taylor J. (2010). Galaxy: a web-based genome analysis tool for experimentalists. Current Protocols in Molecular Biology, Chapter 19: Unit 19.10, 1–21.

  • Briscoe, A. D. (2000). Six opsins from the butterfly Papilio glaucus: molecular phylogenetic evidence for paralogous origins of red-sensitive visual pigments in insects. Journal of Molecular Evolution, 51(2), 110.

    CAS  PubMed  Google Scholar 

  • Briscoe, A. D., & Chittka, L. (2001). The evolution of color vision in insects. Annual Review of Entomology, 46, 471.

    Article  CAS  PubMed  Google Scholar 

  • Briscoe, A. D., Bybee, S. M., Bernard, G. D., Yuan, F., Sison-Mangus, M. P., Reed, R. D., Warren, A. D., Llorente-Bousquets, J., & Chiao, C.-C. (2010). Positive selection of a duplicated UV-sensitive visual pigment coincides with wing pigment evolution in Heliconius butterflies. Proceedings of the National Academy of Sciences of the United States of America, 107(8), 3628.

    Article  PubMed  PubMed Central  Google Scholar 

  • Burkhardt, D. & de la Motte I. (1972). Electrophysiological studies on the eyes of Diptera, Mecoptera and Hymenoptera. Information Processing in the Visual Systems of Arthropods: 147–153.

  • Burrows, M. (2011). Jumping mechanisms and performance of snow fleas (Mecoptera, Boreidae). Journal of Experimental Biology, 214(14), 2362–2374.

    Article  PubMed  Google Scholar 

  • Bybee, S. M., Johnson, K. K., Gering, E. J., Whiting, M. F., & Crandall, K. A. (2012). All the better to see you with: a review of odonate color vision with transcriptomic insight into the odonate eye. Organisms Diversity & Evolution, 12(3), 241.

    Article  Google Scholar 

  • Byers, G. W. (1955). A new species of Boreus (Mecoptera: Boreidae) from Colorado. Occasional Papers of the Museum of Zoology: University of Michigan, 562, 1–4.

  • Byers, G. W. (1969). Ecological and geographical relationships of southern Appalachian Mecoptera (Insecta). The Distributional History of the Southern Appalachians. Part I: Invertebrates. Reseach Division Monograph, 1, 265–276.

  • Byers, G. W. (1993). Autumnal Mecoptera of southeastern United States. The University of Kansas Science Bulletin, 55(2), 57–96.

    Google Scholar 

  • Byers, G. W. (2011). Additions to the Mecoptera of Mexico. Journal of the Kansas Entomological Society, 84(1), 1–11.

    Article  Google Scholar 

  • Byers, G. W., & Thornhill, R. (1983). Biology of the Mecoptera. Annual Review of Entomology, 28(1), 203–228.

    Article  Google Scholar 

  • de Serres, M. (1815). Memoir upon the compound and smooth or simple eyes of insects, and on the manner in which these two species of eyes concur in vision. The New England Journal of Medicine, Surgery and Collateral Branches of Science, 4(2), 141–151.

    Article  Google Scholar 

  • Doering, T. F., Skellern, M., Watts, N., & Cook, S. M. (2012). Colour choice behaviour in the pollen beetle Meligethes aeneus (Coleoptera: Nitidulidae). Physiological Entomology, 37(4), 360–378.

    Article  Google Scholar 

  • Engqvist, L., & Sauer, K. P. (2002). Amorous scorpionflies: causes and consequences of the long pairing prelude of Panorpa cognata. Animal Behaviour, 63, 667.

    Article  Google Scholar 

  • Esben-Petersen, P. (1921). Mecoptera. Coll Selys Longchamps Bruxelles, 5(2), 1.

    Google Scholar 

  • Everett, A., Tong, X., Briscoe, A. D., & Monteiro, A. (2012). Phenotypic plasticity in opsin expression in a butterfly compound eye complements sex role reversal. BMC Evolutionary Biology, 12, 232.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ferris, G. F., & Rees, B. E. (1939). The morphology of Panorpa nuptialis Gerstaecker (Mecoptera: Panorpidae). Microentomology Stanford University, 4, 79.

    Google Scholar 

  • Friedrich, F., Pohl, H., Beckmann, F., & Beutel, R. G. (2013). The head of Merope tuber (Meropeidae) and the phylogeny of Mecoptera (Hexapoda). Athropod Structure & Development, 42(1), 69–88.

    Article  Google Scholar 

  • Giardine, B., Riemer, C., Hardison, R. C., Burhans, R., Elnitski, L., Shah, P., Zhang, Y., Blankenberg, D., Albert, I., & Taylor, J. (2005). Galaxy: a platform for interactive large-scale genome analysis. Genome Research, 15(10), 1451–1455.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goecks, J., Nekrutenko, A., & Taylor, J. (2010). Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biology, 11(8), R86.

    Article  PubMed  PubMed Central  Google Scholar 

  • Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R., & Zeng, Q. (2011). Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology, 29(7), 644–652.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Issiki, S. (1933). Morphological studies on the Panorpidae of Japan and adjoining countries and comparison with American and European forms. Japanese Journal of Zoology, 4, 315.

    Google Scholar 

  • Jennings, D. T., & Sferra, N. J. (2002). An arthropod predator-prey-kleptoparasite association. Northeastern Naturalist, 9(3), 325.

    Article  Google Scholar 

  • Karalius, V., & Buda, V. (2007). Colour vision in currant clearwing moth (Synanthedon tipuliformis) (Lepidoptera: Sesiidae). Acta Zoologica Lituanica, 17(3), 198.

    Article  Google Scholar 

  • Kashiyama, K., Seki, T., Numata, H., & Goto, S. G. (2009). Molecular characterization of visual pigments in Branchiopoda and the evolution of opsins in Arthropoda. Molecular Biology and Evolution, 26(2), 299–311.

    Article  CAS  PubMed  Google Scholar 

  • Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. (outlines version 7). Molecular Biology and Evolution, 30, 772–780.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kiefer, F., Arnold, K., Künzli, M., Bordoli, L., & Schwede, T. (2009). The SWISS-MODEL Repository and associated resources. Nucleic Acids Research, 37(suppl 1), D387–D392.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kofler, R., Orozco-terWengel, P., De Maio, N., Pandey, R. V., Nolte, V., Futschik, A., Kosiol, C., & Schlotterer, C. (2011). PoPoolation: a toolbox for population genetic analysis of next generation sequencing data from pooled individuals. PLoS ONE, 6(1), 15925.

    Article  Google Scholar 

  • Krzeminski, W., & Soszynska-Maj, A. (2012). A new genus and species of scorpionfly (Mecoptera) from Baltic amber, with an unusually developed postnotal organ. Systematic Biology, 37(1), 223–228.

    Google Scholar 

  • Margulies, M., Egholm, M., Altman, W., Attiya, S., Bader, J., Bemben, L., Berka, J., Braverman, M., Chen, Y., Chen, Z., Dewell, S., Du, L., Fierro, J., Gomes, X., Godwin, B., He, W., Helgesen, S., Ho, C., Ho, C., Irzyk, G., Jando, S., Alenquer, M., Jarvie, T., Jirage, K., Kim, J., Knight, J., Lanza, J., Leamon, J., Lefkowitz, S., Lei, M., Li, J., Lohman, K., Lu, H., Makhijani, V., McDade, K., Mckenna, M., Myers, E., Nickerson, E., Nobile, J., Plant, R., Puc, B., Ronan, M., Roth, G., Sarkis, G., Simons, J., Simpson, J., Srinivasan, M., Tartaro, K., Tomasz, A., Vogt, K., Volkmer, G., Wang, S., Wang, Y., Weiner, M., Yu, P., Begley, R., & Rothberg, J. (2005). Genome sequencing in microfabricated high-density picolitre reactors. Nature, 437, 376–380.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Misof, B., Erpenbeck, D., & Sauer, K. P. (2000). Mitochondrial gene fragments suggest paraphyly of the genus Panorpa (Mecoptera, Panorpidae). Molecular Phylogenetics and Evolution, 17(1), 76–84.

    Article  CAS  PubMed  Google Scholar 

  • Ogawa, Y., Awata, H., Wakakuwa, M., Kinoshita, M., Stavenga, D. G., & Arikawa, K. (2012). Coexpression of three middle wavelength-absorbing visual pigments in sexually dimorphic photoreceptors of the butterfly Colias erate. Journal of Comparative Physiology A-Neuroethology Sensory Neural and Behavioral Physiology, 198(12), 857–867.

    Article  CAS  Google Scholar 

  • Penny, N. D., & Byers, G. W. (1979). A check-list of the Mecoptera of the world. Acta Amazonica, 9(2), 365–388.

    Google Scholar 

  • Porter, M. L., Blasic, J. R., Bok, M. J., Cameron, E. G., Pringle, T., Cronin, T. W., & Robinson, P. R. (2011). Shedding new light on opsin evolution. Proceedings of the Royal Socity B: Biological Sciences. doi:10.1098/rspb.2011.1819.

    Google Scholar 

  • Rivera, A. S., Pankey, M. S., Plachetzki, D. C., Villacorta, C., Syme, A. E., Serb, J. M., Omilian, A. R., & Oakley, T. H. (2010). Gene duplication and the origins of morphological complexity in pancrustacean eyes, a genomic approach. BMC Evolutionary Biology, 10, 123.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sison-Mangus, M. P., Bernard, G. D., Lampel, J., & Briscoe, A. D. (2006). Beauty in the eye of the beholder: the two blue opsins of lycaenid butterflies and the opsin gene-driven evolution of sexually dimorphic eyes. Journal of Experimental Biology, 209(16), 3079.

    Article  CAS  PubMed  Google Scholar 

  • Snodgrass, R. (1935). Principles of Insect Morphology (1st ed.). New York and London: McGraw-Hill Book Company.

  • Spaethe, J., & Briscoe, A. D. (2004). Early duplication and functional diversification of the opsin gene family in insects. Molecular Biology and Evolution, 21(8), 1583.

    Article  CAS  PubMed  Google Scholar 

  • Speiser, D. I., Pankey, M. S., Zaharoff, A. K., Battelle, B. A., Bracken-Grissom, H. D., Breinholt, J. W., Bybee, S. M., Cronin, T. W., Garm, A., Lindgren, A. R., Patel, N. H., Porter, M. L., Protas, M. E., Rivera, A. S., Serb, J. M., Zigler, K. S., Crandall, K. A., & Oakley, T. H. (2014). Using phylogenetically-informed annotation (PIA) to search for light-interacting genes in transcriptomes from non-model organisms. Bioinformatics, 15(350), 1471–2105.

    Google Scholar 

  • Stamatakis, A. P., Meier, H., & Ludwig, T. (2008). RAxML: A parallel program for phylogenetic tree inference. See http://sco.h-its.org/exelixis/software.html

  • Taylor, J. S., & Raes, J. (2004). Duplication and divergence: the evolution of new genes and old ideas. Annual Review of Genetics, 38, 615.

    Article  CAS  PubMed  Google Scholar 

  • Taylor, S. D., de la Cruz, K. D., Porter, M. L., & Whiting, M. F. (2005). Characterization of the long-wavelength opsin from Mecoptera and Siphonaptera: does a flea see? Molecular Biology and Evolution, 22(5), 1165–1174.

    Article  CAS  PubMed  Google Scholar 

  • Thornhill, R. (1980a). Competition and coexistence among Panorpa scorpionflies (Mecoptera—Panorpidae). Ecological Monographs, 50(2), 179.

    Article  Google Scholar 

  • Thornhill, R. (1980b). Rape in Panorpa scorpionflies and a general rape hypothesis. Animal Behaviour, 28, 52.

    Article  Google Scholar 

  • Thornhill, R. (1981). Panorpa (Mecoptera, Panorpidae) scorpionflies—systems for understanding resource-defense polygyny and alternative male reproductive efforts. Annual Review of Ecology and Systematics, 12, 355.

    Article  Google Scholar 

  • Whiting, M. F. (2002). Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zoologica Scripta, 31(1), 93–104.

    Article  Google Scholar 

  • Whiting, M. F., Carpenter, J. C., Wheeler, Q. D., & Wheeler, W. C. (1997). The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Systematic Biology, 46(1), 1–68.

    CAS  PubMed  Google Scholar 

  • Zhong, W., & Hua, B. Z. (2013). Mating behaviour and copulatory mechanism in the scorpionfly Neopanorpa longiprocessa (Mecoptera: Panorpidae). Plos One, 8(9), e74781.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We would like to thank Ryan Manwaring and Nick Davis for specimen collection and Heather Bracken-Grissom, Gavin Martin, and Derek Houston (Dept. of Biology, BYU, Provo, UT) for the 454 and Illumina library preparation. We also thank the BYU DNA Sequencing center and the Microarray and Genomic Analysis Core Facility at the Huntsman Cancer Institute at the University of Utah for transcriptome sequencing. We want to thank BYU for access to the Fulton Supercomputer, as well as the Oakley lab for access to and assistance with the PIA pipeline. We also thank the Bybee and Whiting labs (BYU, Provo, UT) for revising this manuscript. This research was supported by a graduate fellowship for BYU to KFM and grant number DEB-1265714 awarded by the National Science Foundation (SMB).

Author information

Authors and Affiliations

  1. Department of Biology, Brigham Young University, 4102 LSB, Provo, UT, 84602, USA

    Katie F. Manwaring, Michael F. Whiting, Edward Wilcox & Seth M. Bybee

Authors
  1. Katie F. Manwaring
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael F. Whiting
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Edward Wilcox
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Seth M. Bybee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Katie F. Manwaring.

Ethics declarations

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Conflict of interest

The authors declare that they have no competing interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Manwaring, K.F., Whiting, M.F., Wilcox, E. et al. A study of common scorpionfly (Mecoptera: Panorpidae) visual systems reveals the expression of a single opsin. Org Divers Evol 16, 201–209 (2016). https://doi.org/10.1007/s13127-015-0241-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13127-015-0241-7

Keywords

Search

Navigation