The evolution of red color vision is linked to coordinated rhodopsin tuning in lycaenid butterflies

Research output: Contribution to journalArticle

Abstract

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.

Details

Authors
  • Marjorie A. Liénard
  • Gary D. Bernard
  • Andrew Allen
  • Jean Marc Lassance
  • Siliang Song
  • Richard Rabideau Childers
  • Nanfang Yu
  • Dajia Ye
  • Adriana Stephenson
  • Wendy A. Valencia-Montoya
  • Shayla Salzman
  • Melissa R.L. Whitaker
  • Michael Calonje
  • Feng Zhang
  • Naomi E. Pierce
Organisations
External organisations
  • Broad Institute
  • University of Washington
  • University of Michigan
  • Columbia University
  • University of Pennsylvania
  • Cornell University
  • ETH Zürich
  • Montgomery Botanical Center
  • Massachusetts Institute of Technology
  • Howard Hughes Medical Institute
  • Harvard University
Research areas and keywords

Subject classification (UKÄ) – MANDATORY

  • Evolutionary Biology

Keywords

  • Ecological adaptation, Insects, Molecular evolution, Spectral sensitivity, Visual system
Original languageEnglish
Article numbere2008986118
JournalProceedings of the National Academy of Sciences of the United States of America
Volume118
Issue number6
Publication statusPublished - 2021
Publication categoryResearch
Peer-reviewedYes