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Parallelism of Amino Acid Changes at the RH1 Affecting Spectral Sensitivity Among Deep-Water Cichlids from Lakes Tanganyika and Malawi

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Parallelism of Amino Acid Changes at the RH1 Affecting Spectral Sensitivity Among Deep-Water Cichlids from Lakes Tanganyika and Malawi Parallelism of amino acid changes at the RH1 affecting spectral sensitivity among deep-water cichlids from Lakes Tanganyika and Malawi Tohru Sugawara*, Yohey Terai*, Hiroo Imai†, George F. Turner‡, Stephan Koblmu¨ ller§, Christian Sturmbauer§, Yoshinori Shichida†, and Norihiro Okada*¶ʈ *Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, 4259 Nagatsuta-cho, Midori-ku, Yokohama 226-8501, Japan; †Department of Biophysics, Graduate School of Science, Kyoto University and Core Research for Evolutional Science and Technology, Japan Science and Technology Corporation, Kyoto 606-8502, Japan; ‡Department of Biological Sciences, University of Hull, Hull HU6 7RX, United Kingdom; §Department of Zoology, Karl Franzens University of Graz, Universitatsplatz 2, A-8010 Graz, Austria; and ¶Division of Cell Fusion, National Institute of Basic Biology, Nishigonaka 38, Myodaiji, Okazaki 444-8585, Japan Edited by Tomoko Ohta, National Institute of Genetics, Mishima, Japan, and approved March 7, 2005 (received for review July 27, 2004) Many examples of the appearance of similar traits in different focus on one of those genes, a rhodopsin, RH1, which is an lineages are known during the evolution of organisms. However, excellent candidate to test for evolutionary parallelism, because the underlying genetic mechanisms have been elucidated in very repeated amino acid replacements occurring at multiple posi- few cases. Here, we provide a clear example of evolutionary tions were suggested to have arisen convergently as functional parallelism, involving changes in the same genetic pathway, pro- adaptation (22). viding functional adaptation of RH1 pigments to deep-water hab- Visual pigment is a seven-transmembrane ␣-helical protein itats during the adaptive radiation of East African cichlid fishes. We that contains a light-absorbing chromophore, retinal (23, 24). determined the RH1 sequences from 233 individual cichlids. The Vertebrate visual pigments are classified into five groups in the reconstruction of cichlid RH1 pigments with 11-cis-retinal from 28 phylogenetic tree (25), and one of the groups is called Rh or sequences showed that the absorption spectra of the pigments of RH1, to which rhodopsins, visual pigments in rod photoreceptor nine species were shifted toward blue, tuned by two particular cells responsible for scotopic (twilight) vision, belong (25, 26). amino acid replacements. These blue-shifted RH1 pigments might The absorption spectrum of a visual pigment can be altered by have evolved as adaptations to the deep-water photic environ- amino acid substitutions within the protein moiety of the visual ment. Phylogenetic evidence indicates that one of the replace- pigment, and key replacement positions are located close to the ments, A292S, has evolved several times independently, inducing retinal-binding pocket (26–28). The chromophore is 11-cis al- similar functional change. The parallel evolution of the same dehyde of either vitamin A1 (retinaldehyde) or vitamin A2 mutation at the same amino acid position suggests that the (3,4-didehydroretinaldehyde) (23). Red-shifts of 10–40 nm can number of genetic changes underlying the appearance of similar be achieved by changing chromophores from A1 to A2 (29). traits in cichlid diversification may be fewer than previously The evolution of visual pigments serves as a prime model for expected. the study of molecular adaptation in vertebrates (26, 28), and several such cases have been reported in primates (30), birds rhodopsin ͉ adaptation (26), and fishes (31, 32). For example, color vision in primates shows a correlation between molecular adaptation and ecolog- orphologically and functionally similar characters often ical specialization (33–35) in that spectral sensitivity of eyes Mevolve more than once because of the operation of match the animal’s environment, allowing for the processing of similar selective pressures in different lineages of organisms. greater amounts of information. The visual system of the Co- One of the fundamental questions concerning character sim- moran coelacanth (32) and deep-water Cottoid fishes in Lake ilarity is whether the genetic mechanisms underlying similar Baikal (31) have rod cells in which the peak sensitivity of visual pigments is blue-shifted to a range of 470–490 nm, because evolutionary changes are the same or are different. Similar longer and short wavelengths are more rapidly attenuated with evolutionary changes caused by the same genetic mechanism increasing water depth, and blue-green light (470–490 nm) are the result of parallelism, whereas those changes produced penetrates to the greatest depth in clear-water habitats (36). by different mechanisms are because of convergence (1). Aquatic environments provide a great diversity of photic con- Although a few cases of both parallelism and convergence in ditions, varying in aspects such as turbidity, color, and brightness Drosophila pigmentation have been recently observed (2–4), (28). The purpose of our study was to investigate the evolution the genetic bases of the appearance of similar characters of the RH1 gene in cichlid fishes of the East African Great Lakes largely remain to be elucidated. in the course of their adaptation to various lacustrine habitats. In East Africa, Lakes Victoria and Malawi harbor endemic Ϸ cichlid fish communities comprising 450–700 species, whereas Materials and Methods Lake Tanganyika holds Ϸ250 species (5). These communities are DNA Sequencing and Sequence Analysis. Determination of the ecologically and morphologically highly diverse but encompass cichlid RH1 gene was as described (22). Nucleotide sequences relatively low genetic diversity, particularly in Malawi and Vic- were deposited in GenBank under accession nos. AB084924– toria (6–11). Cichlids are becoming a model system for under- AB084947, AB185213–AB185242, AB185390, and AB196147. standing the genetic basis of vertebrate speciation (12, 13). Parallel appearances of similar feeding morphologies (8, 14) and nuptial coloration (15) in different lakes or lineages have been This paper was submitted directly (Track II) to the PNAS office. documented. The repeated evolution of similarly adapted cichlid Data deposition: The sequences reported in this paper have been deposited in the GenBank species in various lineages in the same lake or even in different database (accession nos.AB084924–AB084947, AB185213–AB185242, AB185390, and lakes presents an opportunity to explore the issue of convergence AB196147). and parallelism. Recently, several studies of genes underlying the ʈTo whom correspondence should be addressed. E-mail: [email protected]. diversity of cichlids have been reported (12, 16–21). Here, we © 2005 by The National Academy of Sciences of the USA 5448–5453 ͉ PNAS ͉ April 12, 2005 ͉ vol. 102 ͉ no. 15 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0405302102 Downloaded by guest on September 27, 2021 Table 1. The informative positions of amino acid replacements among 28 cichlid RH1 genes, with ␭max values Read vertically, the top three lines specify the amino acid positions in the cichlid RH1 pigment. A dot indicates an amino acid identical to the RH1 consensus. Open boxes at the top indicate the positions of the seven transmembrane regions. Shaded columns indicate the amino acid replacements that line the EVOLUTION chromophore-binding pockets or are in close proximity to the chromophore. The position of residues in each helix is based on the model of Baldwin (61) and on the crystal structure of bovine rhodopsin (62). Comparison of Absorption Spectra of Cichlid RH1 Pigments. RH1 Results coding sequences were amplified by means of PCR using the Sequence Analysis of Cichlid RH1 Genes. We sequenced the RH1 cichlid genome as template with a pair of PCR primers desig- partial coding region (924 bp corresponding to amino acids nated RH1HindIIIF and RH1KpnIR (see Supporting Materials 13–320 among 354 of the full-length of the cichlid RH1 and Methods, which is published as supporting information on protein) of 56 species (Fig. 4, which is published as supporting the PNAS web site). PCR products were digested with KpnI and information on the PNAS web site). Among all sequences, 56 HindIII, and fragments were cloned into a pFLAG-CMV-5a amino acid positions were variable, 42 positions were within (Sigma-Aldrich, St. Louis) expression vector. Their expression the region of transmembrane helices, and 7 positions were and characterization was performed according to the method of close to the retinal-binding pocket. The other 14 variable Ueyama et al. (ref. 37, and for procedural details, see Supporting positions were within the region of extracellular loops, and 2 Materials and Methods). positions were close to the retinal-binding pocket (Table 1). Chromophore Use. Adult cichlids were dark-adapted for 12 h, then Absorption Spectra. To test the relationships between the absorp- decapitated and enucleated. Retinal was extracted from crude tion spectra and ecology, we reconstructed RH1 pigments and eye-cup homogenates or isolated retina as an oxime, as described measured the absorption spectra for 28 cichlid species from (refs. 38–40, and for procedural details, see Supporting Materials African rivers and the three Great Lakes. First, we examined the and Methods). chromophore usage in laboratory-bred individuals of a Victorian ‘‘Haplochromis sp.’’ and the Malawian Dimidiochromis compres- Construction of RH1 Mutants. In vitro mutagenesis of the RH1 was siceps. The ratio of A1 to A2 was revealed to be Ϸ10:1 (data
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