Nocturnal light environments influence color vision and signatures of selection on the OPN1SW opsin gene in nocturnal lemurs

Molecular Biology and Evolution

Volumn 30, Issue 6, 2013, Pages 1420-1437

  Veilleux, Carrie C ^a   Louis, Edward E ^b   Bolnick, Deborah A ^a  

^a University of Texas   (United States)

^b Henry Doorly Zoo   (United States)

Author keywords

ecological genetics; opsin genes; primate evolution; selection

Indexed keywords

OPSIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANOPY; CHEIROGALEUS MEDIUS; COLOR VISION; ENVIRONMENTAL FACTOR; GENE; GENE SEQUENCE; GENETIC ANALYSIS; LEMURIDAE; NIGHT; NOCTURNAL ANIMAL; NONHUMAN; OPN1SW GENE; ORTHOLOGY; PHANER; PHYLOGENY; POPULATION GENETICS; RETINA CONE;

EID: 84877753222     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/mst058     Document Type: Article

References (113)

1. Abdulaev NG, Ridge KD. 2005. Structural and functional aspects of the mammalian rod-cell photoreceptor rhodopsin. In: Briggs WR, Spudich JL, editors. Handbook of photosensory receptors. New York: Wiley-VCH. p. 77-92.
2. Ahnelt PK, Kolb H. 2000. The mammalian photoreceptor mosaic-adaptive design. Prog Retin Eye Res. 19:711-777.
3. Akashi H. 1999. Within- and between-species DNA sequence variation and the "footprint" of natural selection. Gene 238:39-51.
4. Andriaholinirina N, Fausser J-L, Roos C, et al. (20 co-authors). 2006. Molecular phylogeny and taxonomic revision of the sportive lemurs (Lepilemur, Primates). BMC Evol Biol. 6:17.
5. Andriantompohavana R, Lei R, Zaonarivelo JR, et al. (11 co-authors). Molecular phylogeny and taxonomic revision of the woolly lemurs, genus Avahi (Primates: Lemuriformes). Lubbock (TX): Museum of Texas Tech University.
6. Andriantompohavana R, Zaonarivelo JR, Engberg SE, Randriamampiona R, McGuire SM, Shore GD, Rakotonomenjanahary R, Brenneman RA, Louis EE. 2006. Mouse lemurs of northwestern Madagascar with a description of a new species at Lokobe Special Reserve. Occas Pap Tex Tech Univ Mus. 259:1-23.
7. Anisimova M, Nielsen R, Yang Z. 2007. Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics 164:1229-1236.
8. Ankel-Simons F, Rasmussen DT. 2008. Diurnality, nocturnality, and the evolution of primate visual systems. Am J Phys Anthropol. 137: 100-117.
9. Berry V, Semple C. 2006. Fast computation of supertrees for compatible phylogenies with nested taxa. Syst Biol. 55:270-288.
10. Bradley KJ, Cavaco BM, Bowl MR, Harding B, Young A, Thakker RV. 2005. Utilisation of a cryptic non-canonical donor splice site of the gene encoding PARAFIBROMIN is associated with familial isolated primary hyperparathyroidism. J Med Genet. 42:e51-e51.
11. Burset M, Seledtsov IA, Solovyev VV. 2000. Analysis of canonical and non-canonical splice sites inmammalian genomes. Nucleic Acids Res. 28:4364-4375.
12. Cartmill M. 1992. New views on primate origins. Evol Anthropol. 1: 105-111.
13. Carvalho LS, Davies WL, Robinson PR, Hunt DM. 2012. Spectral tuning and evolution of primate short-wavelength-sensitive visual pigments. Proc Biol Sci. 279:387-393.
14. Chamary J, Hurst LD. 2005. Evidence for selection on synonymous mutations affecting stability ofmRNA secondary structure inmammals. Genome Biol. 6:R75.
15. Chatterjee S, Callaway EM. 2002. S cone contributions to the magnocellular visual pathway in macaque monkey. Neuron 35: 1135-1146.
16. Chiu MI, Zack DJ, Wang Y, Nathans J. 1994. Murine and bovine blue cone pigment genes: Cloning and characterization of two newmembers of the s family of visual pigments. Genomics 21:440-443.
17. Choi Y, Sims GE, Murphy S, Miller JR, Chan AP. 2012. Predicting the functional effect of amino acid substitutions and indels. PLoS One 7: E46688.
18. CummingsME. 2004. Modelling divergence in luminance and chromatic detection performance across measured divergence in surfperch (Embiotocidae) habitats. Vision Res. 44:1127-1145.
19. Doi T, Molday RS, Khorana HG. 1990. Role of the intradiscal domain in rhodopsin assembly and function. Proc Natl Acad Sci U S A. 87: 4991-4995.
20. Dominy NJ, Lucas PW. 2004. Significance of color, calories, and climate to the visual ecology of catarrhines. Am J Primatol. 62:189-207.
21. Endler JA. 1993. The color of light in forests and its implications. Ecol Monogr. 63:2-27.
22. Eshleman J, Malhi R, Johnson J, Kaestle F, Lorenz J, Smith D. 2011. Mitochondrial DNA and prehistoric settlements: Native migrations on the western edge of North America. Hum Biol. 76:55-75.
23. Ewens WJ. 1983. The role of models in the analysis of molecular genetic data, with particular reference to restriction fragment data. In: Weir B, Dekker M, editors. Statistical analysis of DNA sequence data. New York: Marcel Dekker. p. 45-74.
24. Fabre P-H, Rodrigues A, Douzery EJP. 2009. Patterns of macroevolution among primates inferred from a supermatrix of mitochondrial and nuclear DNA. Mol Phylogenet Evol. 53:808-825.
25. Fasick JI, Applebury ML, Oprian DD. 2002. Spectral tuning in the mammalian short-wavelength sensitive cone pigments. Biochemistry 41: 6860-6865.
26. Fietz J, Dausmann KH. 2006. Big is beautiful-fat storage and hibernation as a strategy to cope with marked seasonality in the fat-tailed dwarf lemur (Cheirogaleus medius). In: Gould L, editor. Lemurs: Ecology and adaptation. New York: Springer. p. 97-110.
27. Fietz J, Ganzhorn JU 1999. Feeding ecology of the hibernating primate Cheirogaleus medius: How does it get so fat? Oecologia 121:157-164.
28. Ganzhorn JU. 1988. Food partitioning among Malagasy primates. Oecologia 75:436-450.
29. Ganzhorn JU. 1989. Primate species separation in relation to secondary plant chemicals. Hum Evol. 4:125-132.
30. Ganzhorn JU, Abraham J, Razanahoera-Rakotomalala M. 1985. Some aspects of the natural history and food selection of Avahi laniger. Primates 26:452-463.
31. Génin FGS, Masters JC, Ganzhorn JU 2010. Gummivory in cheirogaleids: Primitive retention or adaptation to hypervariable environments?. In: Burrows AM, Nash LT, editors. The evolution of exudativory in primates New York: Springer. p. 123-140.
32. Godfrey LR, Jungers WL. 2003. The extinct sloth lemurs of Madagascar. Evol Anthropol. 12:252-263.
33. Gould L, Sauther M, Cameron A. 2011. Lemuriformes. In: Campbell CJ, Fuentes A, MacKinnon KC, Panger M, Bearder S, editors. Primates in perspective, 2nd ed. Oxford: Oxford University Press. p. 55-79.
34. Griebel U, Peichl L. 2003. Colour vision in aquatic mammals: Facts and open questions. Aquat Mammals 29:18-30.
35. Hall TA. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 41:95-98.
36. Hapke A, Andrianaivo TBD, Gligor M, Razafimahatratra E. 2013. Range shifts of mouse lemurs in south-eastern Madagascar: Evidence from mitochondrial genetic data. In: Masters J, Gamba M, Ge'nin FGS, editors. Leaping ahead: Advances in prosimian biology. New York: Springer New York. p. 71-77.
37. He X, Xu L, Liu Y, Zeng Y 2004. Identification of a novel HLA-F allele - HLA-F 010102. Tissue Antigens 63:181-183.
38. Hladik A. 1980. The dry forest of the west coast of Madagascar: Climate, phenology, and food available for prosimians. In: Charles-Dominique P, Cooper HM, Hladik A, Pariente G, Petter-Rousseaux A, Schilling A, editors. Nocturnal Malagasy primates: Ecology, physiology, and behavior. New York: Academic Press. p. 3-40.
39. Hladik CM, Charles-Dominique P, Petter JJ. 1980. Feeding strategies of five nocturnal prosimians in the dry forest of the west coast of Madagascar. In: Charles-Dominique P, Cooper HM, Hladik A, Pariente G, Petter-Rousseaux A, Schilling A, editors. Nocturnal Malagasy primates: Ecology, physiology, and behaviour. New York: Academic Press. p. 41-73.
40. Hunt DM, Cowing JA, Patel R, Appukuttan B, Bowmaker JK,Mollon JD. 1995. Sequence and evolution of the blue cone pigment gene in old and new world primates. Genomics 27:535-538.
41. Jacobs GH. 2008. Primate color vision: A comparative perspective. Vis Neurosci. 25:619-633.
42. Jacobs GH. 2013. Losses of functional opsin genes, short-wavelength cone photopigments, and color vision-A significant trend in the evolution of mammalian vision. Vis Neurosci. pp. 1-15; Epub ahead of print.
43. Jacobs GH, Deegan JF II, Tan Y, Li W-H. 2002. Opsin gene and photopigment polymorphism in a prosimian primate. Vision Res. 42:11-18.
44. Jacobs GH, Neitz M, Neitz J. 1996. Mutations in S-cone pigment genes and the absence of colour vision in two species of nocturnal primate. Proc Biol Sci. 263:705-710.
45. Johnsen S, Kelber A, Warrant E, Sweeney AM, Widder EA, Lee RL, Hernandez-Andres J. 2006. Crepuscular and nocturnal illumination and its effects on color perception by the nocturnal hawkmoth Deilephila elpenor. J Exp Biol. 209:789-800.
46. Kappeler PM, Rasoloarison RM, Razafimanantsoa L, Walter L, Roos C. 2005. Morphology, behavior and molecular evolution of giant mouse lemurs (Mirza spp.) Gray, 1870, with description of a new species. Primate Rep. 71:3-26.
47. Kawamura S, Kubotera N. 2004. Ancestral Loss of short wave-sensitive cone visual pigment in lorisiform prosimians, contrasting with its strict conservation in other prosimians. J Mol Evol. 58:314-321.
48. Kelber A, Balkenius A, Warrant EJ. 2002. Scotopic colour vision in nocturnal hawkmoths. Nature 419:922-925.
49. Kelber A, Roth LSV. 2006. Nocturnal colour vision: Not as rare as we might think. J Exp Biol. 209:781-788.
50. Kirk EC. 2004. Comparativemorphology of the eye in primates. Anat Rec A Discov Mol Cell Evol Biol. 281:1095-1103.
51. Kirk EC, Simons EL. 2001. Diets of fossil primates from the Fayum depression of Egypt: A quantitative analysis of molar shearing. J Hum Evol. 40:203-229.
52. Kreitman M. 2000. Methods to detect selection in populations with applications to the human. Annu Rev GenomHum Genet. 1:539-559.
53. Li W, DeVries SH. 2006. Bipolar cell pathways for color and luminance vision in a dichromatic mammalian retina. Nat Neurosci. 9: 669-675.
54. Li Z, He S. 2009. Relaxed purifying selection of rhodopsin gene within a Chinese endemic cavefish genus Sinocyclocheilus (Pisces: Cypriniformes). Hydrobiologia 624:139-149.
55. Librado P, Rozas J. 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451-1452.
56. Louis EE, Engberg SE, Lei R, et al. (15 co-authors). 2006. Molecular and morphological analyses of the sportive lemurs (Family Megaladapidae: Genus Lepilemur) reveals 11 previously unrecognized species. Lubbock (TX): Museum of Texas Tech University.
57. Louis EE, Engberg SE, McGuire SM, McCormick MJ, Randriamampionona R, Ranaivoarisoa JF, Bailey CA, Mittermeier RA, Lei R. 2008. Revision of the mouse lemurs, Microcebus (Primates, Lemuriformes), of northern and northwestern Madagascar with descriptions of two new species at Montagne d'Ambre National Park and Antafondro Classified Forest. Primate Conserv. 23:19-38.
58. Maass J, Vose JM, Swank WT, Marti'nez-Yri'zar A. 1995. Seasonal changes of leaf area index (LAI) in a tropical deciduous forest in west Mexico. Forest Ecol Manage. 74:171-180.
59. McDonald JH, KreitmanM. 1991. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652-654.
60. Melin AD,Moritz GL, Fosbury RAE, Kawamura S, Dominy NJ. 2012. Why aye-ayes see blue. Am J Primatol. 74:185-192.
61. Moritz GL, Dominy NJ. 2010. Selective advantages of mono- and dichromatic vision among nocturnal primates. J Vision 10:1-1.
62. Müller B, Glösmann M, Peichl L, Knop GC, Hagemann C, Ammermüller J. 2009. Bat eyes have ultraviolet-sensitive cone photoreceptors. PLoS One 4:e6390.
63. Nathans J, Thomas D, Hogness DS. 1986. Molecular genetics of human color vision: The genes encoding blue, green, and red pigments. Science 232:193-202.
64. Nielsen R. 2005. Molecular signatures of natural selection. Annu Rev Genet. 39:197-218.
65. Norscia I, Ramanamanjato J, Ganzhorn J. 2012. Feeding patterns and dietary profile of nocturnal southern woolly lemurs (Avahi meridionalis) in southeast Madagascar. Int J Primatol. 33:150-167.
66. Palczewski K, Kumasaka T, Hori T, et al. (12 co-authors). 2000. Crystal structure of rhodopsin: A G protein-coupled receptor. Science 289: 739-745.
67. Pariente G. 1980. Quantitative and qualitative study of the light available in the natural biotope of Malagasy prosimians. In: Charles-Dominique P, Cooper HM, Hladik A, Hladik CM, Pages E, Pariente G, Petter-Rousseaux A, Schilling A, editors. Nocturnal Malagasy primates: Ecology, physiology, and behavior. New York: Academic Press. p. 117-134.
68. Partridge JC, Cummings ME. 1999. Adaptation of visual pigments to the aquatic environment. In: Archer SN, Djamgoz M, Loew ER, Partridge JC, Vallerga S, editors. Adaptive mechanisms in the ecology of vision. Boston: Kluwer Academic Publishers. p. 251-283.
69. Peichl L 2005. Diversity of mammalian photoreceptor properties: Adaptations to habitat and lifestyle? Anat Rec A DiscovMol Cell Evol Biol. 287:1001-1012.
70. Peichl L, Behrmann G, Kröger RHH. 2001. For whales and seals the ocean is not blue: A visual pigment loss in marine mammals. Eur J Neurosci. 13:1520-1528.
71. Peichl L, Rakotondraparany F, Kaiser A, Goodman SM, Kappeler PM. 2004. Cone types and distributions in nocturnal and diurnal lemurs of Madagascar. XVI International Congress of Eye Research, Sydney, Australia.
72. Perry GH, Martin RD, Verrelli BC. 2007. Signatures of functional constraint at aye-aye opsin genes: The potential of adaptive color vision in a nocturnal primate. Mol Biol Evol. 24:1963-1970.
73. Perry GH, Pickrell JK. 2010. A rod cell marker of nocturnal ancestry. J Hum Evol. 58:207.
74. Posada D, Crandall KA. 1998. MODELTEST: Testing the model of DNA substitution. Bioinformatics 14:817-818.
75. Poux C, Madsen O, Marquard E, Vieites DR, de Jong WW, Vences M. 2005. Asynchronous colonization of Madagascar by the four endemic clades of primates, tenrecs, carnivores, and rodents as inferred from nuclear genes. Syst Biol. 54:719-730.
76. Radespiel U. 2006. Ecological diversity and seasonal adaptations of mouse lemurs (Microcebus spp.). In: Gould L, Sauther M, editors. Lemurs: Ecology and adaptation. New York: Springer. p. 211-233.
77. R Core Team. 2012. R: A language and environment for statistical computing [Internet]. Version 2.15.2 (2012-10-26). Vienna (Austria): R Foundation for Statistical Computing. Available from: Http://www.Rproject. org/.
78. Rice WR. 1989. Analyzing tables of statistical tests. Evolution 43:223-225.
79. Ronquist F, Teslenko M, Van Der Mark P, et al. (7 co-authors). 2012. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 61:539-542.
80. Roos C, Schmitz J, Zischler H. 2004. Primate jumping genes elucidate strepsirrhine phylogeny. Proc Natl Acad Sci U S A. 101: 10650-10654.
81. Ross CF, Hall MI, Heesy CP. 2007. Were basal primates nocturnal? Evidence from eye and orbit shape. In: Ravosa M, Dagosto M, editors. Primate origins: Adaptation and evolution. New York: Kluwer Academic/Plenum Publishers. p. 233-256.
82. Roth LSV, Kelber A. 2004. Nocturnal colour vision in geckos. Proc Biol Sci. 271:S485-S487.
83. Sakmar TP, Franke RR, Khorana HG. 1989. Glutamic acid-113 serves as the retinylidene Schiff base counterion in bovine rhodopsin. Proc Natl Acad Sci U S A. 86:8309-8313.
84. Santillo S, Orlando P, De Petrocellis L, Cristino L, Guglielmotti V, Musio C. 2006. Evolving visual pigments: Hints from the opsin-based proteins in a phylogenetically old "eyeless" invertebrate. Biosystems 86:3-17.
85. Schneider N, Chikhi L, Currat M, Radespiel U 2010. Signatures of recent spatial expansions in the grey mouse lemur (Microcebus murinus). BMC Evol Biol. 10:105.
86. Schülke O, Kappeler PM. 2003. So near and yet so far: Territorial pairs but low cohesion between pair partners in a nocturnal lemur, Phaner furcifer. Animal Behav. 65:331-343.
87. Seiffert ER, Simons EL, Attia Y. 2003. Fossil evidence for an ancient divergence of lorises and galagos. Nature 422:421-424.
88. Shi Y, Yokoyama S. 2003. Molecular analysis of the evolutionary significance of ultraviolet vision in vertebrates. Proc Natl Acad Sci U S A. 100:8308-8313.
89. Silveira L, Kremers J, Lee B, Martin P. 2005. Comparative anatomy and physiology of the primate retina. In: Kremers J, editor. The primate visual system: A comparative approach. Hoboken (NJ): John Wiley. p. 127-160.
90. Spady TC, Seehausen O, Loew ER, Jordan RC, Kocher TD, Carleton KL. 2005. Adaptive molecular evolution in the opsin genes of rapidly speciating cichlid species. Mol Biol Evol. 22:1412-1422.
91. Srinivas M, Ng L, Liu H, Jia L, Forrest D. 2006. Activation of the blue opsin gene in cone photoreceptor development by retinoid-related orphan receptor b. Mol Endocrinol. 20:1728-1741.
92. Sussman RW. 1995. How primates invented the rainforest and vice versa. In: Alterman L, Doyle G, Izark M, editors. Creatures of the dark: The nocturnal prosimians. New York: Plenum Press. p. 1-10.
93. Swofford DL. 2003. PAUP Phylogenetic analysis using parsimony (and other methods). Sunderland (MA): Sinauer Associates.
94. Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.
95. Tan Y, Yoder AD, Yamashita N, Li W-H. 2005. Evidence from opsin genes rejects nocturnality in ancestral primates. Proc Natl Acad Sci U S A. 102:14712-14716.
96. Thalmann U. 2001. Food resource characteristics in two nocturnal lemurs with different social behavior: Avahi occidentalis and Lepilemur edwardsi. Int J Primatol. 22:287-324.
97. Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JAM. 2007. Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res. 35:W71-W74.
98. Veilleux CC, Cummings ME. 2012. Nocturnal light environments and species ecology: Implications for nocturnal color vision in forests. J Exp Biol. 215:4085-4096.
99. Walls GL. 1942. The vertebrate eye and its adaptive radiation. Bloomfield Hills (MI): The Cranbrook Press.
100. Warrant E. 2004. Vision in the dimmest habitats on Earth. J Comp Physiol A. 190:765-789.
101. Warren RD, Crompton RH. 1997. A comparative study of the ranging behaviour, activity rhythms and sociality of Lepilemur edwardsi (Primates, Lepilemuridae) and Avahi occidentalis (Primates, Indriidae) at Ampijoroa, Madagascar. J Zool. 243:397-415.
102. Watterson GA. 1975. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 7:256-276.
103. Wells NA. 2003. Some hypotheses on the Mesozoic and Cenozoic paleoenvironmental history of Madagascar. In: Goodman SM, Benstead J, editors. The natural history of Madagascar. Chicago: The University of Chicago Press. p. 16-34.
104. Wilbanks AM, Laporte SA, Bohn LM, Barak LS, Caron MG. 2002. Apparent loss-of-function mutant GPCRs revealed as constitutively desensitized receptors. Biochemistry 41:11981-11989.
105. Xia X. 2001. Data analysis in molecular biology and evolution. Boston: Kluwer Academic Publishers.
106. Xia X, Xie Z. 2001. DAMBE: Software package for data analysis in molecular biology and evolution. J Hered. 92:371-373.
107. Yang Z. 1998. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol. 15: 568-573.
108. Yang Z. 2007. PAML 4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol. 24:1586-1591.
109. Yang Z, Nielsen R, Goldman N, Pedersen A-MK. 2000. Codon-substitution models for heterogenous selection pressure at amino acid sites. Genetics 155:431-449.
110. Yoder AD, Yang Z. 2004. Divergence dates for Malagasy lemurs estimated from multiple gene loci: Geological and evolutionary context. Mol Ecol. 13:757-773.
111. Zaramody A, Fausser J-L, Roos C, Zinner D, Andriaholinirina N, Rabarivola C, Norscia I, Tattersall I, Rumpler Y. 2006. Molecular phylogeny and taxonomic revision of the eastern woolly lemurs (Avahi laniger). Primate Rep. 74:9-24.
112. Zhao H, Rossiter SJ, Teeling EC, Li C, Cotton JA, Zhang S. 2009. The evolution of color vision in nocturnal mammals. Proc Natl Acad Sci U S A. 106:8980-8985.
113. Zhao H, Xu D, Zhou Y, Flanders J, Zhang S. 2009. Evolution of opsin genes reveals a functional role of vision in the echolocating little brown bat (Myotis lucifugus). Biochem Syst Ecol. 37:154-161.