Adaptive evolution of color vision as seen through the eyes of butterflies

  1. Francesca D. Frentiu*,
  2. Gary D. Bernard,
  3. Cristina I. Cuevas*,
  4. Marilou P. Sison-Mangus*,
  5. Kathleen L. Prudic, and
  6. Adriana D. Briscoe*,§
  1. *Comparative and Evolutionary Physiology Group, Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697;
  2. Department of Electrical Engineering, University of Washington, Seattle, WA 98195; and
  3. Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721
  1. Fig. 1.

    Butterfly compound eye and opsin expression patterns. (A) Diagram of a longitudinal section through the compound eye showing the ommatidial units. Black dots indicate location of photoreceptor nuclei. R, retina; L, lamina; M, medulla. (B) Schematic of an ommatidium. C, cornea; CC, crystalline cone; n, nuclei; 9, the ninth photoreceptor cell that sits just above the basement membrane. (C) Opsin mRNA expression patterns. The cross-sections of three ommatidia are shown. The cross-hatched area in the middle of each depicts the fused microvillous membranes of the rhabdomeres that contain the visual pigment proteins. Numbers refer to the photoreceptor cells (R1–R8), and the colors refer to the opsin expression patterns: violet, UV opsin mRNA; blue, blue opsin; green, long-wavelength opsin. Modified from Sauman et al. (35).


  2. Fig. 2.

    Normalized absorbance spectra of L photopigments in the Limenitis genus measured by epimicrospectrophotometry. Idealized spectra (solid curves) based on the 1987 Bernard template (56). λmax values are shown in upper right corner. R545 from L. arthemis astyanax: dots represent dorsal retina, and triangles represent ventral retina.


  3. Fig. 3.

    Character mapping of L photopigment λmax values onto an L opsin gene tree. Numbers shown above branch indicate maximum-likelihood bootstrap support values and numbers below branch show Bayesian clade credibility values. Thick black lines indicate nymphalid branches along which blue spectral shifts occurred that were investigated in the parallel/convergent change and branch-site tests of selection. Nodes in which ancestral state reconstructions shown in Table 3 were performed are indicated by letters.


  4. Fig. 4.

    Topographical and homology models of L. arthemis astyanax L opsin. (A) Topographical opsin map showing amino acid differences (filled circles) between L. arthemis astyanax and L. archippus archippus opsins. The diagram is based on a model of bovine rhodopsin (46). Dashed line indicates boundaries of alignment used in phylogenetic analyses. The amino acid residues are numbered relative to the alignment shown in SI Fig. 5. Black arrows, amino acid sites under positive selection. (B) Homology model of L. arthemis astyanax L opsin, with chromophore shown (arrow). (C) Candidate spectral tuning sites that directly face the chromophore (11-cis-retinal).


Footnotes

  • §To whom correspondence should be addressed. E-mail: abriscoe{at}uci.edu
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