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Coexpression of three middle wavelength-absorbing visual pigments in sexually dimorphic photoreceptors of the butterfly Colias erate

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Abstract

The tiered ommatidia of the Eastern Pale Clouded yellow butterfly, Colias erate, contain nine photoreceptor cells, four of which contribute their rhabdomeral microvilli to the distal tier of the rhabdom. We analyzed the visual pigments and spectral sensitivities of these distal photoreceptors in both sexes of Colias erate. A subset of photoreceptor cells expresses a newly discovered middle wavelength-absorbing opsin, C olias e rate Blue (CeB), in addition to two previously described middle wavelength-absorbing opsins, CeV1 and CeV2. The other photoreceptors either coexpress CeV1 and CeV2, or exclusively express a short wavelength-absorbing opsin, CeUV, or a long wavelength-absorbing opsin, CeL. Males and females have the same visual pigment expression patterns, but the photoreceptor spectral sensitivities are sexually dimorphic. The photoreceptors coexpressing three middle wavelength-absorbing opsins are broad-blue receptors in males, but in females they are narrow-blue receptors. Those with CeV1 and CeV2 are violet receptors in females, while they are shouldered-blue receptors in males. The sexual dimorphism in spectral sensitivity is caused by a sex-specific distribution of fluorescent pigment that functions as a spectral filter.

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Abbreviations

bB:

Broad blue

bG:

Broad green

CeB:

Colias erate blue-absorbing opsin

CeL:

Colias erate long wavelength-absorbing opsin

CeUV:

Colias erate ultraviolet-absorbing opsin

CeV1:

Colias erate violet-absorbing opsin 1

CeV2:

Colias erate violet-absorbing opsin 2

nB:

Narrow blue

sB:

Shouldered blue

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Acknowledgments

We thank Dr. Atsushi Nagayama who provided help in acquiring Catopsilia pomona, and Dr. Finlay Stewart for checking the English. YO was a recipient of a JSPS (Japan Society for the Promotion of Science) student fellowship (DC2). The work was supported in part by the JSPS Grants-in-Aid for Scientific Research No. 21247009 to KA, the MAFF (Ministry of Agriculture, Forestry and Fisheries of Japan) grant (Elucidation of biological mechanisms of photoresponse and development of advanced technologies utilizing light) No. INSECT-1101 to KA, and by a grant from the CPIS (Sokendai Center for the Promotion of Integrated Sciences) to HA, and by AFOSR/EOARD grant FA8655-08-1-3012 to DGS. All experiments were conducted according to the MEXT (Ministry of Education, Culture, Sports, Science and Technology of Japan) guidelines for proper conduct of animal experiment and related activities in academic research institutions.

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Authors and Affiliations

  1. Laboratory of Neuroethology, Sokendai-Hayama (The Graduate University for Advanced Studies), Hayama, 240-0193, Japan

    Yuri Ogawa, Hiroko Awata, Motohiro Wakakuwa, Michiyo Kinoshita & Kentaro Arikawa

  2. Computational Physics, University of Groningen, 9747 AG, Groningen, The Netherlands

    Doekele G. Stavenga

Authors
  1. Yuri Ogawa
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  2. Hiroko Awata
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  3. Motohiro Wakakuwa
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  4. Michiyo Kinoshita
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  5. Doekele G. Stavenga
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  6. Kentaro Arikawa
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Corresponding author

Correspondence to Kentaro Arikawa.

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Ogawa, Y., Awata, H., Wakakuwa, M. et al. Coexpression of three middle wavelength-absorbing visual pigments in sexually dimorphic photoreceptors of the butterfly Colias erate . J Comp Physiol A 198, 857–867 (2012). https://doi.org/10.1007/s00359-012-0756-8

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