[en] Color vision has evolved multiple times in both vertebrates and invertebrates and is largely determined by the number and variation in spectral sensitivities of distinct opsin subclasses. However, because of the difficulty of expressing long-wavelength (LW) invertebrate opsins in vitro, our understanding of the molecular basis of functional shifts in opsin spectral sensitivities has been biased toward research primarily in vertebrates. This has restricted our ability to address whether invertebrate Gq protein-coupled opsins function in a novel or convergent way compared to vertebrate Gt opsins. Here we develop a robust heterologous expression system to purify invertebrate rhodopsins, identify specific amino acid changes responsible for adaptive spectral tuning, and pinpoint how molecular variation in invertebrate opsins underlie wavelength sensitivity shifts that enhance visual perception. By combining functional and optophysiological approaches, we disentangle the relative contributions of lateral filtering pigments from red-shifted LW and blue short-wavelength opsins expressed in distinct photoreceptor cells of individual ommatidia. We use in situ hybridization to visualize six ommatidial classes in the compound eye of a lycaenid butterfly with a four-opsin visual system. We show experimentally that certain key tuning residues underlying green spectral shifts in blue opsin paralogs have evolved repeatedly among short-wavelength opsin lineages. Taken together, our results demonstrate the interplay between regulatory and adaptive evolution at multiple Gq opsin loci, as well as how coordinated spectral shifts in LW and blue opsins can act together to enhance insect spectral sensitivity at blue and red wavelengths for visual performance adaptation.
Disciplines :
Life sciences: Multidisciplinary, general & others
Author, co-author :
Lienard, Marjorie ; Université de Liège - ULiège > GIGA > GIGA Molecular Biology of Diseases ; Université de Liège - ULiège > Département des sciences de la vie
Bernard, Gary D ; Department of Electrical and Computer Engineering, University of Washington, Seattle, WA 98195
Allen, Andrew; Broad Institute of MIT and Harvard University, Cambridge, MA 02142
Lassance, Jean-Marc ; Université de Liège - ULiège > Département de gestion vétérinaire des Ressources Animales (DRA) > Génomique animale ; Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138
Song, Siliang ; Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138
Childers, Richard Rabideau ; Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138
Yu, Nanfang ; Department of Applied Physics and Applied Mathematics, Columbia University, New York, NY 10027
Ye, Dajia; Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138
Stephenson, Adriana; Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138
Valencia-Montoya, Wendy A ; Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138
Salzman, Shayla ; Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138
Whitaker, Melissa R L ; Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138
Calonje, Michael; Montgomery Botanical Center, Miami, FL 33156
Zhang, Feng; Broad Institute of MIT and Harvard University, Cambridge, MA 02142 ; Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139 ; Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139 ; McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, MA 02139 ; Howard Hughes Medical Institute, Cambridge, MA 02139
Pierce, Naomi E ; Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, marjorie.lienard@biol.lu.se npierce@oeb.harvard.edu
NSF - National Science Foundation [US-VA] [US-VA] NHGRI - National Human Genome Research Institute [US-MD] [US-MD] NHLBI - National Heart Lung and Blood Institute [US-MD] [US-MD] NIMH - National Institute of Mental Health [US-MD] [US-MD] KAW - Knut och Alice Wallenbergs Stiftelse [SE] Kungliga Fysiografiska Sällskapet i Lund [SE] Stiftelsen Lars Hiertas Minne [SE]
Funding text :
We thank Masaru Hojo for providing pupae of A. japonica; Sandy Koi for providing E. atala and for advice regarding rearing and ecology; Maria Eriksson and Peg Coughin for assistance with electron microscopy; Xi Shi, Sara Jones, and Jonathan Schmid-Burgk for advice on cell culture; Ian Slaymaker for advice on protein purification procedures; Hopi E. Hoekstra for access to cryostat and microscope; Rachel Gaudet and Jos? Velilla for guidance using Pymol; Rosalie Crouch for providing the 11-cis-retinal; Jeanne M. Serb and Davide Faggionato for advice on 11-cis-retinal delivery; Kentaro Arikawa, Julien Ayroles, Gregor Belu?i?, Mary Caswell Stoddard, Almut Kelber, Olle Lind, Rhiannon Macrae, Samuel Aravinthan, and Mandyam Veerambudi Srinivasan for helpful discussions; Adriana Briscoe for providing helpful feedback on an earlier version of the manuscript; and Richard Belliveau, Maggie Starvish, and Rachel Hawkins for providing logistical support. The computations were run on the FASRC Odyssey cluster of the FAS Division of Science Research Computing Group at Harvard University. This work was supported by a Mind Brain Behavior Interfaculty grant (to N.E.P. and M.A.L.), an Knut and Alice Wallenberg postdoctoral fellowship at the Broad Institute of MIT and Harvard (to M.A.L.), the Royal Physiographic Society of Lund (M.A.L.), the Lars Hierta Memorial Foundation (M.A.L.), an NSF graduate research fellowship (to S. Salzman), personal funds (G.D.B.), and NSF DEB-1541560 (to N.E.P.) and PHY-1411445 (to N.E.P. and N.Y.). F.Z. is an investigator of the Howard Hughes Medical Institute and is supported by NIH Grants 1R01-HG009761, 1R01-MH110049, and 1DP1-HL141201; the Open Philanthropy Project; the Harold G. and Leila Mathers and the Edward Mallinckrodt, Jr. Foundations; the Poitras Center for Psychiatric Disorders Research at MIT; the Hock E. Tan and K. Lisa Yang Center for Autism Research at MIT; and by the Phillips family and J. and P. Poitras. Publication charges supported by a grant from the Wetmore Colles Fund.ACKNOWLEDGMENTS. We thank Masaru Hojo for providing pupae of A. japonica; Sandy Koi for providing E. atala and for advice regarding rearing and ecology; Maria Eriksson and Peg Coughin for assistance with electron microscopy; Xi Shi, Sara Jones, and Jonathan Schmid-Burgk for advice on cell culture; Ian Slaymaker for advice on protein purification procedures; Hopi E. Hoekstra for access to cryostat and microscope; Rachel Gaudet and José Velilla for guidance using Pymol; Rosalie Crouch for providing the 11-cis-retinal; Jeanne M. Serb and Davide Faggionato for advice on 11-cis-retinal delivery; Kentaro Arikawa, Julien Ayroles, Gregor Belušicˇ, Mary Caswell Stoddard, Almut Kelber, Olle Lind, Rhiannon Macrae, Samuel Aravinthan, and Mandyam Veerambudi Srinivasan for helpful discussions; Adriana Briscoe for providing helpful feedback on an earlier version of the manuscript; and Richard Belliveau, Maggie Starvish, and Rachel Hawkins for providing logistical support. The computations were run on the FASRC Odyssey cluster of the FAS Division of Science Research Computing Group at Harvard University. This work was supported by a Mind Brain Behavior Interfaculty grant (to N.E.P. and M.A.L.), an Knut and Alice Wallenberg postdoctoral fellowship at the Broad Institute of MIT and Harvard (to M.A.L.), the Royal Physiographic Society of Lund (M.A.L.), the Lars Hierta Memorial Foundation (M.A.L.), an NSF graduate research fellowship (to S. Salzman), personal funds (G.D.B.), and NSF DEB-1541560 (to N.E.P.) and PHY-1411445 (to N.E.P. and N.Y.). F.Z. is an investigator of the Howard Hughes Medical Institute and is supported by NIH Grants 1R01-HG009761, 1R01-MH110049, and 1DP1-HL141201; the Open Philanthropy Project; the Harold G. and Leila Mathers and the Edward Mallinckrodt, Jr. Foundations; the Poitras Center for Psychiatric Disorders Research at MIT; the Hock E. Tan and K. Lisa Yang Center for Autism Research at MIT; and by the Phillips family and J. and P. Poitras. Publication charges supported by a grant from the Wetmore Colles Fund.
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