Convergent selection pressures drive the evolution of rhodopsin kinetics at high altitudes via nonparallel mechanisms

Aho, 1988, Low retinal noise in animals with low body temperature allows high visual sensitivity, Nature, 334, 348, 10.1038/334348a0

Aminetzach, 2009, Convergent evolution of novel protein function in shrew and lizard venom, Curr. Biol., 19, 1925, 10.1016/j.cub.2009.09.022

Anisimova, 2007, The quest for natural selection in the age of comparative genomics, Heredity, 99, 567, 10.1038/sj.hdy.6801052

Anisimova, 2001, Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution, Mol. Biol. Evol., 18, 1585, 10.1093/oxfordjournals.molbev.a003945

Åqvist, 2017, Cold adaptation of triosephosphate isomerase, Biochemistry, 56, 4169, 10.1021/acs.biochem.7b00523

Beall, 2007, Two routes to functional adaptation: Tibetan and Andean high-altitude natives, Proc. Natl. Acad. Sci. USA, 104, 8655, 10.1073/pnas.0701985104

Bielawski, 2004, A maximum likelihood method for detecting functional divergence at individual codon sites, with application to gene family evolution, J. Mol. Evol., 59, 121, 10.1007/s00239-004-2597-8

Bofkin, 2007, Variation in evolutionary processes at different codon positions, Mol. Biol. Evol., 24, 513, 10.1093/molbev/msl178

Brodie, 2010, Convergent evolution: pick your poison carefully, Curr. Biol., 20, 152, 10.1016/j.cub.2009.12.029

Castiglione, 2017, Evolution of nonspectral rhodopsin function at high altitudes, Proc. Natl. Acad. Sci., 114, 7385, 10.1073/pnas.1705765114

Chen, 1997, Convergent evolution of antifreeze glycoproteins in Antarctic notothenioid fish and Arctic cod, Proc. Natl. Acad. Sci. USA, 94, 3817, 10.1073/pnas.94.8.3817

Chen, 2013, Evolutionary origin and early biogeography of otophysan fishes (Ostariophysi: Teleostei), Evolution, 67, 2218, 10.1111/evo.12104

Cheviron, 2014, Integrating evolutionary and functional tests of adaptive hypotheses: a case study of altitudinal differentiation in hemoglobin function in an Andean sparrow, Zonotrichia capensis, Mol. Biol. Evol., 31, 2948, 10.1093/molbev/msu234

Chikina, 2016, Hundreds of genes experienced convergent shifts in selective pressure in marine mammals, Mol. Biol. Evol., 33, 2182, 10.1093/molbev/msw112

Cortesi, 2015, Ancestral duplications and highly dynamic opsin gene evolution in percomorph fishes, Proc. Natl. Acad. Sci. USA, 112, 1493, 10.1073/pnas.1417803112

Dungan, 2017, Epistatic interactions influence terrestrial-marine functional shifts in cetacean rhodopsin, Proc. R. Soc. B Biol. Sci., 284, 10.1098/rspb.2016.2743

Dungan, 2016, Spectral tuning of killer whale (Orcinus orca) rhodopsin: evidence for positive selection and functional adaptation in a cetacean visual pigment, Mol. Biol. Evol., 33, 323, 10.1093/molbev/msv217

Ebrey, 2001, Vertebrate photoreceptors, Prog. Retin. Eye Res., 20, 49, 10.1016/S1350-9462(00)00014-8

Elde, 2009, Protein kinase R reveals an evolutionary model for defeating viral mimicry, Nature, 457, 485, 10.1038/nature07529

Endler, 1986, Natural selection in the wild

Ernst, 2014, Microbial and animal rhodopsins: structures, functions, and molecular mechanisms, Chem. Rev., 114, 126, 10.1021/cr4003769

Feldman, 2012, Constraint shapes convergence in tetrodotoxin-resistant sodium channels of snakes, Proc. Natl. Acad. Sci., 109, 4556, 10.1073/pnas.1113468109

Fields, 2015, Adaptations of protein structure and function to temperature: there is more than one way to “skin a cat, J. Exp. Biol., 218, 1801, 10.1242/jeb.114298

Foote, 2015, Convergent evolution of the genomes of marine mammals, Nat. Genet., 47, 272, 10.1038/ng.3198

Frederiksen, 2016, Rhodopsin kinase and arrestin binding control the decay of photoactivated rhodopsin and dark adaptation of mouse rods, J. Gen. Physiol., 148, 1, 10.1085/jgp.201511538

Govardovskii, 2000, In search of the visual pigment template, Vis. Neurosci., 17, 509, 10.1017/S0952523800174036

Gozem, 2012, The molecular mechanism of thermal noise in rod photoreceptors, Science, 337, 1225, 10.1126/science.1220461

Gregory-Wodzicki, 2000, Uplift history of the central and northern Andes: a review, GSA Bull, 112, 1091, 10.1130/0016-7606(2000)112<1091:UHOTCA>2.0.CO;2

Guo, 2005, Phylogeny and biogeography of Chinese sisorid catfishes re-examined using mitochondrial cytochrome b and 16S rRNA gene sequences, Mol. Phylogenet. Evol., 35, 344, 10.1016/j.ympev.2004.12.015

Guo, 2014, Unusual kinetics of thermal decay of dim-light photoreceptors in vertebrate vision, Proc. Natl. Acad. Sci. USA, 111, 10438, 10.1073/pnas.1410826111

Hauser, 2017, Accelerated evolution and functional divergence of the dim light visual pigment accompanies cichlid colonization of Central America, Mol. Biol. Evol., 34, 2650, 10.1093/molbev/msx192

Hayes, 1999, Natural selection on thermogenic capacity of high-altitude deer mice, Evolution, 53, 1280, 10.1111/j.1558-5646.1999.tb04540.x

Hedges, 2015, Tree of life reveals clock-like speciation and diversification, Mol. Biol. Evol., 32, 835, 10.1093/molbev/msv037

Hofmann, 2009, A G protein-coupled receptor at work: the rhodopsin model, Trends Biochem. Sci., 34, 540, 10.1016/j.tibs.2009.07.005

Horvath, 1993, Atmospheric light absorption-a review, Atmos. Environ. A Gen. Top., 27, 293, 10.1016/0960-1686(93)90104-7

Hughes, 2006, Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes, Proc. Natl. Acad. Sci. USA, 103, 10334, 10.1073/pnas.0601928103

Hunt, 2001, The molecular basis for spectral tuning of rod visual pigments in deep-sea fish, J. Exp. Biol., 204, 3333, 10.1242/jeb.204.19.3333

Imai, 1997, Single amino acid residue as a functional determinant of rod and cone visual pigments, Proc. Natl. Acad. Sci. USA, 94, 2322, 10.1073/pnas.94.6.2322

Imai, 2007, Molecular properties of rhodopsin and rod function, J. Biol. Chem., 282, 6677, 10.1074/jbc.M610086200

Jessen, 1991, Adaptation of bird hemoglobins to high altitudes: demonstration of molecular mechanism by protein engineering, Proc. Natl. Acad. Sci. USA, 88, 6519, 10.1073/pnas.88.15.6519

Kefalov, 2003, Role of visual pigment properties in rod and cone phototransduction, Nature, 425, 526, 10.1038/nature01992

Kochendoerfer, 1999, How color pigments are tuned, Trends Biochem. Sci., 24, 300, 10.1016/S0968-0004(99)01432-2

Körner, 2007, The use of “altitude” in ecological research, Trends Ecol. Evol., 22, 569, 10.1016/j.tree.2007.09.006

Lamb, 2016, Evolution of vertebrate phototransduction: cascade activation, Mol. Biol. Evol., 33, 2064, 10.1093/molbev/msw095

Losos, 2011, Convergence, adaptation, and constraint, Evolution, 65, 1827, 10.1111/j.1558-5646.2011.01289.x

Löytynoja, 2008, Phylogeny-aware gap placement prevents errors in sequence alignment and evolutionary analysis, Science, 320, 1632, 10.1126/science.1158395

Lujan, 2015, Extremophile fishes: ecology, evolution, and physiology of teleosts in extreme environments, 107, 10.1007/978-3-319-13362-1_6

Luk, 2016, Modulation of thermal noise and spectral sensitivity in Lake Baikal cottoid fish rhodopsins, Sci. Rep., 6, 10.1038/srep38425

Ma, 2016, Comprehensive transcriptome analysis of six catfish species from an altitude gradient reveals adaptive evolution in Tibetan fishes, G3, 6, 1, 10.1534/g3.115.024448

Manceau, 2010, Convergence in pigmentation at multiple levels: mutations, genes and function, Philos. Trans. R. Soc. B Biol. Sci., 365, 2439, 10.1098/rstb.2010.0104

McGlothlin, 2016, Historical contingency in a multigene family facilitates adaptive evolution of toxin resistance, Curr. Biol., 26, 1616, 10.1016/j.cub.2016.04.056

Morrow, 2017, An experimental comparison of human and bovine rhodopsin provides insight into the molecular basis of retinal disease, FEBS Lett, 591, 1720, 10.1002/1873-3468.12637

Natarajan, 2016, Predictable convergence in hemoglobin function has unpredictable molecular underpinnings, Science, 354, 336, 10.1126/science.aaf9070

Nevado, 2016, Widespread adaptive evolution during repeated evolutionary radiations in New World lupins, Nat. Commun., 7, 10.1038/ncomms12384

Nguyen, 2016, Evolutionary drivers of thermoadaptation in enzyme catalysis, Science, 355, 289, 10.1126/science.aah3717

Niemiller, 2013, Evidence for repeated loss of selective constraint in rhodopsin of amblyopsid cavefishes (teleostei: Amblyopsidae), Evolution, 67, 732, 10.1111/j.1558-5646.2012.01822.x

Okada, 2004, The retinal conformation and its environment in rhodopsin in light of a new 2.2 Å crystal structure, J. Mol. Biol., 342, 571, 10.1016/j.jmb.2004.07.044

Palczewski, 2006, G protein-coupled receptor rhodopsin, Annu. Rev. Biochem., 75, 743, 10.1146/annurev.biochem.75.103004.142743

Parker, 2013, Genome-wide signatures of convergent evolution in echolocating mammals, Nature, 502, 1, 10.1038/nature12511

Partha, 2017, Subterranean mammals show convergent regression in ocular genes and enhancers, along with adaptation to tunneling, eLife, 6, 10.7554/eLife.25884

Patel, 2012, Convergent evolution of escape from hepaciviral antagonism in primates, PLoS Biol, 10, e1001282, 10.1371/journal.pbio.1001282

Peng, 2004, Phylogenetic relationships of glyptosternoid fishes (Siluriformes: Sisoridae) inferred from mitochondrial cytochrome b gene sequences, Mol. Phylogenet. Evol., 31, 979, 10.1016/j.ympev.2003.10.023

Peng, 2006, Uplift of the Tibetan plateau: evidence from divergence times of glyptosternoid catfishes, Mol. Phylogenet. Evol., 39, 568, 10.1016/j.ympev.2005.10.016

Projecto-Garcia, 2013, Repeated elevational transitions in hemoglobin function during the evolution of Andean hummingbirds, Proc. Natl. Acad. Sci. USA, 110, 20669, 10.1073/pnas.1315456110

Protas, 2006, Genetic analysis of cavefish reveals molecular convergence in the evolution of albinism, Nat. Genet., 38, 107, 10.1038/ng1700

Rosenblum, 2010, Molecular and functional basis of phenotypic convergence in white lizards at White Sands, Proc. Natl. Acad. Sci. USA, 107, 2113, 10.1073/pnas.0911042107

Royden, 2008, The geological evolution of the Tibetan plateau, Science, 321, 1054, 10.1126/science.1155371

Rubin, 2016, Comparative genomics reveals convergent rates of evolution in ant-plant mutualisms, Nat. Commun., 7

Schaefer, 2011, Historical biogeography of neotropical freshwater fishes, 259

Schaefer, 2010, Rivers as islands: determinants of the distribution of Andean astroblepid catfishes, J. Fish Biol., 77, 2373, 10.1111/j.1095-8649.2010.02822.x

Schaefer, 2011, Nucleotide sequence data confirm diagnosis and local endemism of variable morphospecies of Andean astroblepid catfishes (Siluriformes: Astroblepidae), Zool. J. Linn. Soc., 162, 90, 10.1111/j.1096-3642.2010.00673.x

Schafer, 2016, Decay of an active GPCR: conformational dynamics govern agonist rebinding and persistence of an active, yet empty, receptor state, Proc. Natl. Acad. Sci., 113, 11961, 10.1073/pnas.1606347113

Schott, 2014, Divergent positive selection in rhodopsin from lake and riverine cichlid fishes, Mol. Biol. Evol., 31, 1149, 10.1093/molbev/msu064

Siddiqui, 2006, Cold-adapted enzymes, Annu. Rev. Biochem., 75, 403, 10.1146/annurev.biochem.75.103004.142723

Sommaruga, 1999, Dissolved organic carbon concentration and phytoplankton biomass in high-mountain lakes of the Austrian Alps: potential effect of climatic warming an UV underwater attenuation, Arct. Antarct. Alp. Res., 31, 247, 10.2307/1552253

Stern, 2013, The genetic causes of convergent evolution, Nat. Rev. Genet., 14, 751, 10.1038/nrg3483

Stojanovic, 2003, Retinitis pigmentosa rhodopsin mutations L125R and A164V perturb critical interhelical interactions: new insights through compensatory mutations and crystal structure analysis, J. Biol. Chem., 278, 39020, 10.1074/jbc.M303625200

Storz, 2016, Causes of molecular convergence and parallelism in protein evolution, Nat. Rev. Genet., 17, 239, 10.1038/nrg.2016.11

Storz, 2007, The molecular basis of high-altitude adaptation in deer mice, PLoS Genet, 3, e45, 10.1371/journal.pgen.0030045

Sugawara, 2010, Vertebrate rhodopsin adaptation to dim light via rapid meta-II intermediate formation, Mol. Biol. Evol., 27, 506, 10.1093/molbev/msp252

Sullivan, 2006, A phylogenetic analysis of the major groups of catfishes (Teleostei: Siluriformes) using rag1 and rag2 nuclear gene sequences, Mol. Phylogenet. Evol, 41, 636, 10.1016/j.ympev.2006.05.044

Tenaillon, 2012, The molecular diversity of adaptive convergence, Science, 335, 457, 10.1126/science.1212986

Thomas, 2015, Determining the null model for detecting adaptive convergence from genomic data: a case study using echolocating mammals, Mol. Biol. Evol, 32, 1232, 10.1093/molbev/msv013

Eps, 2017, Conformational equilibria of light-activated rhodopsin in nanodiscs, Proc. Natl. Acad. Sci., 114, E3268, 10.1073/pnas.1620405114

Venkatakrishnan, 2016, Diverse activation pathways in class A GPCRs converge near the G-protein-coupling region, Nature, 536, 484, 10.1038/nature19107

Verberk, 2011, Oxygen supply in aquatic ectotherms: partial pressure and solubility together explain biodiversity and size patterns, Ecology, 92, 1565, 10.1890/10-2369.1

Weadick, 2012, An improved likelihood ratio test for detecting site-specific functional divergence among clades of protein-coding genes, Mol. Biol. Evol., 29, 1297, 10.1093/molbev/msr311

Xie, 2003, An opsin mutant with increased thermal stability, Biochemistry, 42, 1995, 10.1021/bi020611z

Xing, 2017, Uplift-driven diversification in the Hengduan Mountains, a temperate biodiversity hotspot, Proc. Natl. Acad. Sci. USA, 114, E3444, 10.1073/pnas.1616063114

Yang, 2007, PAML 4: phylogenetic analysis by maximum likelihood, Mol. Biol. Evol., 24, 1586, 10.1093/molbev/msm088

Yang, 2005, Bayes empirical Bayes inference of amino acid sites under positive selection, Mol. Biol. Evol., 22, 1107, 10.1093/molbev/msi097

Yokoyama, 2008, Elucidation of phenotypic adaptations: molecular analyses of dim-light vision proteins in vertebrates, Proc. Natl. Acad. Sci. USA, 105, 13480, 10.1073/pnas.0802426105

Yue, 2017, Spontaneous activation of visual pigments in relation to openness/closeness of chromophore-binding pocket, Elife, 6, 1, 10.7554/eLife.18492

Zhou, 2016, Diversification of Sisorid catfishes (Teleostei: Siluriformes) in relation to the orogeny of the Himalayan plateau, Sci. Bull., 61, 991, 10.1007/s11434-016-1104-0

Zou, 2015a, Are convergent and parallel amino acid substitutions in protein evolution more prevalent than neutral expectations, Mol. Biol. Evol., 32, 2085, 10.1093/molbev/msv091

Zou, 2015b, No genome-wide protein sequence convergence for echolocation, Mol. Biol. Evol., 32, 1237, 10.1093/molbev/msv014