In deep-water animals, the visual sensory system is often challenged by the dim-light environment. Here, we focus on the molecular mechanisms involved in rapid deep-water adaptations. We examined visual system evolution in a small-scale yet phenotypically and ecologically diverse adaptive radiation, the species flock of cichlid fishes in deep crater lake Barombi Mbo in Cameroon, West Africa. We show that rapid adaptations of the visual system to the novel deep-water habitat primarily occurred at the level of gene expression changes rather than through nucleotide mutations, which is compatible with the young age of the radiation. Based on retinal bulk RNA sequencing of all eleven species, we found that the opsin gene expression pattern was substantially different for the deep-water species. The nine shallow-water species feature an opsin palette dominated by the red-sensitive (LWS) opsin, whereas the two unrelated deep-water species lack expression of LWS and the violet-sensitive (SWS2B) opsin, thereby shifting the cone sensitivity to the centre of the light spectrum. Deep-water species further predominantly express the green-sensitive RH2Aα over RH2Aβ. We identified one amino acid substitution in the RH2Aα opsin specific to the deep-water species. We finally performed a comparative gene expression analysis in retinal tissue of deep- vs. shallow-water species. We thus identified 46 differentially expressed genes, many of which are associated with functions in vision, hypoxia management or circadian clock regulation, with some of them being associated with human eye diseases.

Department of Biological Sciences University of Ngaoundéré Ngaoundéré Cameroon

Department of Management of Fisheries and Aquatic Ecosystems University of Douala Douala Cameroon

Department of Physiology Charles University Prague Prague Czech Republic

Department of Zoology Charles University Prague Prague Czech Republic

Zoological Institute University of Basel Basel Switzerland

Zobrazit více v PubMed

Albers, C. A., Cvejic, A., Favier, R., Bouwmans, E. E., Alessi, M.-C., Bertone, P., … Ouwehand, W. H. (2011). Exome sequencing identifies NBEAL2 as the causative gene for gray platelet syndrome. Nature Genetics, 43(8), 735. https://doi.org/10.1038/ng.885

Andrews, S. (2010). FastQC: A quality control tool for high throughput sequence data. Retrieved from: http://www.bioinformatics.babraham.ac.uk/projects/fastqc

Baldo, L., Pretus, J. L., Riera, J. L., Musilova, Z., Bitja Nyom, A. R., & Salzburger, W. (2017). Convergence of gut microbiotas in the adaptive radiations of African cichlid fishes. The ISME Journal, 11(9), 1975-1987. https://doi.org/10.1038/ismej.2017.62

Bandelt, H., Forster, P., & Röhl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16(1), 37-48. https://doi.org/10.1093/oxfordjournals.molbev.a026036

Barluenga, M., Stölting, K. N., Salzburger, W., Muschick, M., & Meyer, A. (2006). Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature, 439(7077), 719-723.

Bolger, A. M., Lohse, M., & Usadel, B. (2014). Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30(15), 2114-2120. https://doi.org/10.1093/bioinformatics/btu170

Braasch, I., Gehrke, A. R., Smith, J. J., Kawasaki, K., Manousaki, T., Pasquier, J., … Postlethwait, J. H. (2016). The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons. Nature Genetics, 48(4), 427-437. https://doi.org/10.1038/ng.3526

Brawand, D., Wagner, C. E., Li, Y. I., Malinsky, M., Keller, I., Fan, S., … Di Palma, F. (2014). The genomic substrate for adaptive radiation in African cichlid fish. Nature, 513(7518), 375. https://doi.org/10.1038/nature13726

Brzezinski, J. A., Lamba, D. A., & Reh, T. A. (2010). Blimp1 controls photoreceptor versus bipolar cell fate choice during retinal development. Development, 137(4), 619-629. https://doi.org/10.1242/dev.043968

Brzezinski, J. A., Park, K. U., & Reh, T. A. (2013). Blimp1 (Prdm1) prevents re-specification of photoreceptors into retinal bipolar cells by restricting competence. Developmental Biology, 384(2), 194-204. https://doi.org/10.1016/j.ydbio.2013.10.006

Carleton, K. L. (2009). Cichlid fish visual systems: Mechanisms of spectral tuning. Integrative Zoology, 4(1), 75-86. https://doi.org/10.1111/j.1749-4877.2008.00137.x

Carleton, K. L., Dalton, B. E., Escobar-Camacho, D., & Nandamuri, S. P. (2016). Proximate and ultimate causes of variable visual sensitivities: Insights from cichlid fish radiations. Genesis, 54(6), 299-325. https://doi.org/10.1002/dvg.22940

Carleton, K. L., Hárosi, F. I., & Kocher, T. D. (2000). Visual pigments of African cichlid fishes: Evidence for ultraviolet vision from microspectrophotometry and DNA sequences. Vision Research, 40(8), 879-890. https://doi.org/10.1016/S0042-6989(99)00238-2

Carleton, K. L., & Kocher, T. D. (2001). Cone opsin genes of african cichlid fishes: Tuning spectral sensitivity by differential gene expression. Molecular Biology and Evolution, 18(8), 1540-1550. https://doi.org/10.1093/oxfordjournals.molbev.a003940

Carleton, K. L., Spady, T. C., Streelman, J. T., Kidd, M. R., McFarland, W. N., & Loew, E. R. (2008). Visual sensitivities tuned by heterochronic shifts in opsin gene expression. BMC Biology, 6, 22. https://doi.org/10.1186/1741-7007-6-22

Chen, W. J., Bonillo, C., & Lecointre, G. (2003). Repeatability of clades as a criterion of reliability: A case study for molecular phylogeny of Acanthomorpha (Teleostei) with larger number of taxa. Molecular Phylogenetics and Evolution, 26(2), 262-288. https://doi.org/10.1016/S1055-7903(02)00371-8

Chen, Y., Thompson, D. C., Koppaka, V., Jester, J. V., & Vasiliou, V. (2013). Ocular aldehyde dehydrogenases: Protection against ultraviolet damage and maintenance of transparency for vision. Progress in Retinal and Eye Research, 33, 28-39. https://doi.org/10.1016/j.preteyeres.2012.10.001

Cornen, G., Bande, Y., Giresse, P., & Maley, J. (1992). The nature and chronostratigraphy of Quaternary pyroclastic accumulations from Lake Barombi Mbo (West-Cameroon). Journal of Volcanology and Geothermal Research, 51(4), 357-374. https://doi.org/10.1016/0377-0273(92)90108-P

Corso-Díaz, X., Jaeger, C., Chaitankar, V., & Swaroop, A. (2018). Epigenetic control of gene regulation during development and disease: A view from the retina. Progress in Retinal and Eye Research, 65, 1-27. https://doi.org/10.1016/j.preteyeres.2018.03.002

Cortesi, F., Musilová, Z., Stieb, S. M., Hart, N. S., Siebeck, U. E., Malmstrøm, M., … Salzburger, W. (2015). Ancestral duplications and highly dynamic opsin gene evolution in percomorph fishes. Proceedings of the National Academy of Sciences of the United States of America, 112(5), 1493-1498. https://doi.org/10.1073/pnas.1417803112

Coyne, J. A., & Orr, H. A. (2004). Speciation. Sunderland, MA: Sinauer Associates.

Cruz, N. M., Yuan, Y., Leehy, B. D., Baid, R., Kompella, U., DeAngelis, M. M., … Haider, N. B. (2014). Modifier genes as therapeutics: The nuclear hormone receptor Rev Erb alpha (Nr1d1) rescues Nr2e3 associated retinal disease. PLoS ONE, 9(1), e87942. https://doi.org/10.1371/journal.pone.0087942

Dalton, B. E., Loew, E. R., Cronin, T. W., & Carleton, K. L. (2014). Spectral tuning by opsin coexpression in retinal regions that view different parts of the visual field. Proceedings of the Royal Society B: Biological Sciences, 281(1797), 20141980. https://doi.org/10.1098/rspb.2014.1980

Dennis, Y. T., Chung, I., & Wu, S. M. (2014). Possible roles of glutamate transporter EAAT5 in mouse cone depolarizing bipolar cell light responses. Vision Research, 103, 63-74. https://doi.org/10.1016/j.visres.2014.06.005

Dunz, A. R., & Schliewen, U. K. (2013). Molecular phylogeny and revised classification of the haplotilapiine cichlid fishes formerly referred to as “Tilapia”. Molecular Phylogenetics and Evolution, 68(1), 64-80. https://doi.org/10.1016/j.ympev.2013.03.015

Ebrey, T., & Koutalos, Y. (2001). Vertebrate Photoreceptors. Progress in Retinal and Eye Research, 20(1), 49-94. https://doi.org/10.1016/S1350-9462(00)00014-8

Fernald, R. D. (1981). Chromatic organization of a cichlid fish retina. Vision Research, 21(12), 1749-1753. https://doi.org/10.1016/0042-6989(81)90207-8

Govardovskii, V. I., Fyhrquist, N., Reuter, T., Kuzmin, D. G., & Donner, K. (2000). In search of the visual pigment template. Visual Neuroscience, 17, 509-528. https://doi.org/10.1017/S0952523800174036

Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., … Regev, A. (2011). Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology, 29(7), 644. https://doi.org/10.1038/nbt.1883

Green, J., Corbet, S. A., & Betney, E. (1973). The blood of endemic cichlids in Barombi Mbo in relation to stratification and their feeding habits. Journal of Zoology, 170(3), 299-308.

Han, E. C., Huang, Y. C., Lin, J. M., Lin, H. J., Wu, J. Y., Lee, C. C., & Tsai, F. J. (2012). Association of the PLEKHO2 and PLEKHH1 gene polymorphisms with type 2 diabetic retinopathy in a Taiwanese population. ScienceAsia, 38(4), 340-348. https://doi.org/10.2306/scienceasia1513-1874.2012.38.340

Hofmann, C. M., O'Quin, K. E., Marshall, N. J., Cronin, T. W., Seehausen, O., & Carleton, K. L. (2009). The eyes have it: Regulatory and structural changes both underlie cichlid visual pigment diversity. PLOS Biology, 7(12), e1000266. https://doi.org/10.1371/journal.pbio.1000266

Huang, G., Zhang, F., Ye, Q., & Wang, H. (2016). The circadian clock regulates autophagy directly through the nuclear hormone receptor Nr1d1/Rev-erbα and indirectly via Cebpb/(C/ebpβ) in zebrafish. Autophagy, 12(8), 1292-1309. https://doi.org/10.1080/15548627.2016.1183843

Huang, J., Possin, D. E., & Saari, J. C. (2009). Localizations of visual cycle components in retinal pigment epithelium. Molecular Vision, 15, 223.

Hughes, S., Jagannath, A., Rodgers, J., Hankins, M. W., Peirson, S. N., & Foster, R. G. (2016). Signalling by melanopsin (OPN4) expressing photosensitive retinal ganglion cells. Eye, 30(2), 247-254. https://doi.org/10.1038/eye.2015.264

Jia, L., Oh, E. C., Ng, L., Srinivas, M., Brooks, M., Swaroop, A., & Forrest, D. (2009). Retinoid-related orphan nuclear receptor RORβ is an early-acting factor in rod photoreceptor development. Proceedings of the National Academy of Sciences of the United States of America, 106(41), 17534-17539.

Johnson, S., Michaelides, M., Aligianis, I. A., Ainsworth, J. R., Mollon, J. D., Maher, E. R., … Hunt, D. M. (2004). Achromatopsia caused by novel mutations in both CNGA3 and CNGB3. Journal of Medical Genetics, 41(2), e20. https://doi.org/10.1136/jmg.2003.011437

Katoh, K., & Standley, D. M. (2013). mafft multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30(4), 772-780. https://doi.org/10.1093/molbev/mst010

Kautt, A. F., Elmer, K. R., & Meyer, A. (2012). Genomic signatures of divergent selection and speciation patterns in a “natural experiment”, the young parallel radiations of Nicaraguan crater lake cichlid fishes. Molecular Ecology, 21(19), 4770-4786. https://doi.org/10.1111/j.1365-294X.2012.05738.x

Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., & Salzberg, S. L. (2013). tophat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biology, 14(4), R36. https://doi.org/10.1186/gb-2013-14-4-r36

Koltsova, S. V., Shilov, B., Birulina, J. G., Akimova, O. A., Haloui, M., Kapilevich, L. V., … Orlov, S. N. (2014). Transcriptomic changes triggered by hypoxia: Evidence for HIF-1α-independent,[Na+] i/[K+] i-mediated, excitation-transcription coupling. PLoS ONE, 9(11), e110597. https://doi.org/10.1371/journal.pone.0110597

Kompass, K. S., Agapova, O. A., Li, W., Kaufman, P. L., Rasmussen, C. A., & Hernandez, M. R. (2008). Bioinformatic and statistical analysis of the optic nerve head in a primate model of ocular hypertension. BMC Neuroscience, 9(1), 93. https://doi.org/10.1186/1471-2202-9-93

Lamb, T. D., Collin, S. P., & Pugh, E. N. (2007). Evolution of the vertebrate eye: Opsins, photoreceptors, retina and eye cup. Nature Reviews Neuroscience, 8(12), 960-976. https://doi.org/10.1038/nrn2283

Langmead, B., & Salzberg, S. L. (2012). Fast gapped-read alignment with Bowtie 2. Nature Methods, 9(4), 357-359. https://doi.org/10.1038/nmeth.1923

Leigh, J. W., & Bryant, D. (2015). PopART: Full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6(9), 1110-1116.

Luna, C., Li, G., Huang, J., Qiu, J., Wu, J., Yuan, F., … Gonzalez, P. (2012). Regulation of trabecular meshwork cell contraction and intraocular pressure by miR-200c. PLoS ONE, 7(12), e51688. https://doi.org/10.1371/journal.pone.0051688

Malinsky, M., Challis, R. J., Tyers, A. M., Schiffels, S., Terai, Y., Ngatunga, B. P., … Turner, G. F. (2015). Genomic islands of speciation separate cichlid ecomorphs in an East African crater lake. Science, 350(6267), 1493-1498.

Malinsky, M., Svardal, H., Tyers, A. M., Miska, E. A., Genner, M. J., Turner, G. F., & Durbin, R. (2018). Whole-genome sequences of Malawi cichlids reveal multiple radiations interconnected by gene flow. Nature Ecology & Evolution, 2(12), 1940. https://doi.org/10.1038/s41559-018-0717-x

Maya-Vetencourt, J. F., Tiraboschi, E., Greco, D., Restani, L., Cerri, C., Auvinen, P., … Castrén, E. (2012). Experience-dependent expression of NPAS4 regulates plasticity in adult visual cortex. The Journal of Physiology, 590(19), 4777-4787.

Miller, M. A., Pfeiffer, W., & Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA pp 1-8.

Miyagi, R., Terai, Y., Aibara, M., Sugawara, T., Imai, H., Tachida, H., … Okada, N. (2012). Correlation between nuptial colors and visual sensitivities tuned by opsins leads to species richness in sympatric Lake Victoria cichlid fishes. Molecular Biology and Evolution, 29(11), 3281-3296. https://doi.org/10.1093/molbev/mss139

Mollema, N. J., Yuan, Y., Jelcick, A. S., Sachs, A. J., von Alpen, D., Schorderet, D., … Haider, N. B. (2011). Nuclear receptor Rev-erb alpha (Nr1d1) functions in concert with Nr2e3 to regulate transcriptional networks in the retina. PLoS ONE, 6(3), e17494. https://doi.org/10.1371/journal.pone.0017494

Moreno, J. M., Sousa, V. C., Jesus, T. F., & Coelho, M. M. (2019). Adaptation and convergence in genes of the circadian system in Iberian Squalius freshwater species. bioRxiv, 706713. https://doi.org/10.1101/706713

Morita, M., Ohneda, O., Yamashita, T., Takahashi, S., Suzuki, N., Nakajima, O., … Fujii-Kuriyama, Y. (2003). HLF/HIF-2α is a key factor in retinopathy of prematurity in association with erythropoietin. The EMBO Journal, 22(5), 1134-1146. https://doi.org/10.1093/emboj/cdg117

Morris, A. C., Forbes-Osborne, M. A., Pillai, L. S., & Fadool, J. M. (2011). Microarray analysis of XOPS-mCFP zebrafish retina identifies genes associated with rod photoreceptor degeneration and regeneration. Investigative Ophthalmology & Visual Science, 52(5), 2255-2266. https://doi.org/10.1167/iovs.10-6022

Muschick, M., Indermaur, A., & Salzburger, W. (2012). Convergent evolution within an adaptive radiation of cichlid fishes. Current Biology, 22(24), 2362-2368. https://doi.org/10.1016/j.cub.2012.10.048

Musilova, Z., Cortesi, F., Matschiner, M., Davies, W. I. L. D., Patel, J. S., Stieb, S. M., … Salzburger, W. (2019). Vision using multiple distinct rod opsins in deep-sea fishes. Science, 364(6440), 588-592.

Musilova, Z., Indermaur, A., Nyom, A. R. B., Tropek, R., Martin, C., & Schliewen, U. K. (2014). Persistence of Stomatepia mongo, an endemic cichlid fish of the Barombi Mbo crater lake, southwestern Cameroon, with notes on its life history and behavior. Copeia, 2014(3), 556-560.

Nagai, H., Terai, Y., Sugawara, T., Imai, H., Nishihara, H., Hori, M., & Okada, N. (2011). Reverse evolution in RH1 for adaptation of cichlids to water depth in Lake Tanganyika. Molecular Biology and Evolution, 28(6), 1769-1776. https://doi.org/10.1093/molbev/msq344

Natoli, R., Zhu, Y., Valter, K., Bisti, S., Eells, J., & Stone, J. (2010). Gene and noncoding RNA regulation underlying photoreceptor protection: Microarray study of dietary antioxidant saffron and photobiomodulation in rat retina. Molecular Vision, 16, 1801.

Nelson, R. F., & Singla, N. (2009). A spectral model for signal elements isolated from zebrafish photopic electroretinogram. Visual Neuroscience, 26(4), 349-363. https://doi.org/10.1017/S0952523809990113

O'Carroll, D. C., & Warrant, E. J. (2017). Vision in dim light: Highlights and challenges. Philosophical Transactions of the Royal Society B: Biological Sciences, 372, 20160062.

O'Quin, K. E., Hofmann, C. M., Hofmann, H. A., & Carleton, K. L. (2010). Parallel evolution of opsin gene expression in African cichlid fishes. Molecular Biology and Evolution, 27(12), 2839-2854. https://doi.org/10.1093/molbev/msq171

O'Quin, K. E., Smith, A. R., Sharma, A., & Carleton, K. L. (2011). New evidence for the role of heterochrony in the repeated evolution of cichlid opsin expression. Evolution & Development, 13(2), 193-203. https://doi.org/10.1111/j.1525-142X.2011.00469.x

Panagis, L., Zhao, X., Ge, Y., Ren, L., Mittag, T. W., & Danias, J. (2011). Retinal gene expression changes related to IOP exposure and axonal loss in DBA/2J mice. Investigative Ophthalmology & Visual Science, 52(11), 7807-7816. https://doi.org/10.1167/iovs.10-7063

Parry, J. W. L., Carleton, K. L., Spady, T., Carboo, A., Hunt, D. M., & Bowmaker, J. K. (2005). Mix and match color vision: Tuning spectral sensitivity by differential opsin gene expression in Lake Malawi cichlids. Current Biology, 15, 1734-1739. https://doi.org/10.1016/j.cub.2005.08.010

Pittlik, S., Domingues, S., Meyer, A., & Begemann, G. (2008). Expression of zebrafish aldh1a3 (raldh3) and absence of aldh1a1 in teleosts. Gene Expression Patterns, 8(3), 141-147. https://doi.org/10.1016/j.gep.2007.11.003

Porter, M. L., Roberts, N. W., & Partridge, J. C. (2016). Evolution under pressure and the adaptation of visual pigment compressibility in deep-sea environments. Molecular Phylogenetics and Evolution, 105, 160-165. https://doi.org/10.1016/j.ympev.2016.08.007

Rennison, D. J., Owens, G. L., & Taylor, J. S. (2012). Opsin gene duplication and divergence in ray-finned fish. Molecular Phylogenetics and Evolution, 62(3), 986-1008. https://doi.org/10.1016/j.ympev.2011.11.030

Richards, E. J., Poelstra, J. W., & Martin, C. H. (2018). Don't throw out the sympatric speciation with the crater lake water: Fine-scale investigation of introgression provides equivocal support for causal role of secondary gene flow in one of the clearest examples of sympatric speciation. Evolution Letters, 2(5), 524-540. https://doi.org/10.1002/evl3.78

Ronquist, F., & Huelsenbeck, J. P. (2003). mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572-1574. https://doi.org/10.1093/bioinformatics/btg180

Rozas, J., Ferrer-Mata, A., Sánchez-DelBarrio, J. C., Guirao-Rico, S., Librado, P., Ramos-Onsins, S. E., & Sánchez-Gracia, A. (2017). DnaSP 6: DNA sequence polymorphism analysis of large datasets. Molecular Biology and Evolution, 34, 3299-3302. https://doi.org/10.1093/molbev/msx248

Salzburger, W. (2018). Understanding explosive diversification through cichlid fish genomics. Nature Reviews Genetics, 19, 705-717. https://doi.org/10.1038/s41576-018-0043-9

Santos, M. E., Baldo, L., Gu, L., Boileau, N., Musilova, Z., & Salzburger, W. (2016). Comparative transcriptomics of anal fin pigmentation patterns in cichlid fishes. BMC Genomics, 17, 712. https://doi.org/10.1186/s12864-016-3046-y

Schedel, F. D. B., Musilova, Z., & Schliewen, U. (2019). East African cichlid lineages (Teleostei: Cichlidae) might be older than their ancient host lakes: New divergence estimates for the East African cichlid radiation. BMC Evolutionary Biology, 19(1), 94. https://doi.org/10.1186/s12862-019-1417-0

Schlegel, C. R., Georgiou, M. L., Misterek, M. B., Stöcker, S., Chater, E. R., Munro, C. E., … Costa-Pereira, A. P. (2016). DAPK2 regulates oxidative stress in cancer cells by preserving mitochondrial function. Cell Death & Disease, 6(3), e1671. https://doi.org/10.1038/cddis.2015.31

Schliewen, U. K., & Klee, B. (2004). Reticulate sympatric speciation in Cameroonian crater lake cichlids. Frontiers in Zoology, 1, 5.

Schliewen, U., Tautz, D., & Paabo, S. (1994). Sympatric speciation suggested by monophyly of crater lake cichlids. Nature, 368, 629-632. https://doi.org/10.1038/368629a0

Seehausen, O. (2006). African cichlid fish: a model system in adaptive radiation research. Proceedings of the Royal Society of London B: Biological Sciences, 273(1597), 1987-1998.

Seehausen, O., Terai, Y., Magalhaes, I. S., Carleton, K. L., Mrosso, H. D. J., Miyagi, R., … Okada, N. (2008). Speciation through sensory drive in cichlid fish. Nature, 455(7213), 620-626.

Smith, A. R., van Staaden, M. J., & Carleton, K. L. (2012). An evaluation of the role of sensory drive in the evolution of lake Malawi cichlid fishes. International Journal of Evolutionary Biology, 2012, 647420. https://doi.org/10.1155/2012/647420

Spady, T. C., Parry, J. W. L., Robinson, P. R., Hunt, D. M., Bowmaker, J. K., & Carleton, K. L. (2006). Evolution of the cichlid visual palette through ontogenetic subfunctionalization of the opsin gene arrays. Molecular Biology and Evolution, 23(8), 1538-1547. https://doi.org/10.1093/molbev/msl014

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 β. Molecular Endocrinology, 20(8), 1728-1741. https://doi.org/10.1210/me.2005-0505

Stamatakis, A. (2014). raxml version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30(9), 1312-1313. https://doi.org/10.1093/bioinformatics/btu033

Sugawara, T., Terai, Y., Imai, H., Turner, G. F., Koblmuller, S., Sturmbauer, C., … Okada, N. (2005). Parallelism of amino acid changes at the RH1 affecting spectral sensitivity among deep-water cichlids from Lakes Tanganyika and Malawi. Proceedings of the National Academy of Sciences of the United States of America, 102(15), 5448-5453. https://doi.org/10.1073/pnas.0405302102

Torres-Dowdall, J., Pierotti, M. E. R., Härer, A., Karagic, N., Woltering, J. M., Henning, F., … Meyer, A. (2017). Rapid and parallel adaptive evolution of the visual system of Neotropical Midas cichlid fishes. Molecular Biology and Evolution, 34(10), 2469-2485. https://doi.org/10.1093/molbev/msx143

Townley, I. K., Karchner, S. I., Skripnikova, E., Wiese, T. E., Hahn, M. E., & Rees, B. B. (2016). Sequence and functional characterization of hypoxia-inducible factors, HIF1α, HIF2αa, and HIF3α, from the estuarine fish, Fundulus heteroclitus. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 312(3), R412-R425.

Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D. R., … Pachter, L. (2012). Differential gene and transcript expression analysis of RNA-seq experiments with tophat and cufflinks. Nature Protocols, 7(3), 562. https://doi.org/10.1038/nprot.2012.016

Trewavas, E., Green, J., & Corbet, S. A. (1972). Ecological studies on crater lakes in West Cameroon fishes of Barombi Mbo. Journal of Zoology, 167(1), 41-95. https://doi.org/10.1111/j.1469-7998.1972.tb01722.x

Usui, T., Hara, M., Satoh, H., Moriyama, N., Kagaya, H., Amano, S., … Seki, G. (2001). Molecular basis of ocular abnormalities associated with proximal renal tubular acidosis. The Journal of Clinical Investigation, 108(1), 107-115. https://doi.org/10.1172/JCI11869

Verheyen, E., Salzburger, W., Snoeks, J., & Meyer, A. (2003). Origin of the superflock of cichlid fishes from Lake Victoria, East Africa. Science, 300(5617), 325-329.

Wahlestedt, M., Ladopoulos, V., Hidalgo, I., Sanchez Castillo, M., Hannah, R., Säwén, P., … Bryder, D. (2017). Critical modulation of hematopoietic lineage fate by hepatic leukemia factor. Cell Reports, 21(8), 2251-2263. https://doi.org/10.1016/j.celrep.2017.10.112

Wang, G. L., & Semenza, G. L. (1993). General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proceedings of the National Academy of Sciences of the United States of America, 90(9), 4304-4308. https://doi.org/10.1073/pnas.90.9.4304

Weadick, C. J., & Chang, B. S. W. (2012). Complex patterns of divergence among green-sensitive (RH2a) African cichlid opsins revealed by Clade model analyses. BMC Evolutionary Biology, 12(1), https://doi.org/10.1186/1471-2148-12-206

Weitz, C. J., Miyake, Y., Shinzato, K., Montag, E., Zrenner, E., Went, L. N., & Nathans, J. (1992). Human tritanopia associated with two amino acid substitutions in the blue-sensitive opsin. American Journal of Human Genetics, 50(3), 498-507.

Yokoyama, S. (2008). Evolution of dim-light and color vision pigments. Annual Review of Genomics and Human Genetics, 9, 259-282. https://doi.org/10.1146/annurev.genom.9.081307.164228

All quiet on the western front? The evolutionary history of monogeneans (Dactylogyridae: Cichlidogyrus, Onchobdella) infecting a West and Central African tribe of cichlid fishes (Chromidotilapiini)

Exon-based Phylogenomics and the Relationships of African Cichlid Fishes: Tackling the Challenges of Reconstructing Phylogenies with Repeated Rapid Radiations

Developmental changes of opsin gene expression in ray-finned fishes (Actinopterygii)

Molecular evolution and depth-related adaptations of rhodopsin in the adaptive radiation of cichlid fishes in Lake Tanganyika

Visual Gene Expression Reveals a cone-to-rod Developmental Progression in Deep-Sea Fishes

Adaptive Radiation from a Chromosomal Perspective: Evidence of Chromosome Set Stability in Cichlid Fishes (Cichlidae: Teleostei) from the Barombi Mbo Lake, Cameroon

Zobrazit více v PubMed

GENBANK
SAMN12385063, SAMN12385064, SAMN12385065, SAMN12385066, SAMN12385067, SAMN12385068, SAMN12385069, SAMN12385070, SAMN12385071, SAMN10473299, SAMN10473300, SAMN10473301, SAMN12385075, SAMN12385076, SAMN12385077, SAMN12385078, SAMN12385079, SAMN12385080, SAMN12385081, MKQE00000000.2, MKQE00000000.1, SRX095621, MN258381, MN258511, PRJNA556940, PRJNA421052