[en] Evolutionary transitions in water column usage have played a major role in shaping ray-finned fish diversity. However, the extent to which vision-associated trait complexity and water column usage is coupled remains unclear. Here we investigated the relationship between depth niche, eye size, and the molecular basis of light detection across the Antarctic notothenioid adaptive radiation. Integrating a phylogenetic comparative framework with data on eye size and depth occupancy, we provide support for an acceleration in the rate of eye size diversification nearly 20 million years after the initial radiation. Our results further reveal that levels of eye size divergence are often highest between closely related taxa. We further analyzed opsin tuning site sequences and found changes representing repeated instances of independent tuning site changes across the notothenioid phylogeny that are generally not associated with habitat depth or species eye size. Collectively, our results strongly support that multiple evolutionary pathways underlie the diversification of visual adaptations in this iconic adaptive radiation.
Research Center/Unit :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Yoder, Ella B; Department of Bioinformatics and Genomics University of North Carolina at Charlotte Charlotte North Carolina USA ; Research Triangle High School Durham North Carolina USA
Parker, Elyse; Department of Ecology and Evolutionary Biology Yale University New Haven Connecticut USA
Frederich, Bruno ; Université de Liège - ULiège > Freshwater and OCeanic science Unit of reSearch (FOCUS)
Tew, Alexandra; Department of Bioinformatics and Genomics University of North Carolina at Charlotte Charlotte North Carolina USA
Jones, Christopher D; Ecosystem Science Division NOAA Southwest Fisheries Science Center La Jolla California USA
Dornburg, Alex ; Department of Bioinformatics and Genomics University of North Carolina at Charlotte Charlotte North Carolina USA
Language :
English
Title :
Multiple Pathways of Visual Adaptations for Water Column Usage in an Antarctic Adaptive Radiation
Abrams, P. A. 2014. “How Precautionary Is the Policy Governing the Ross Sea Antarctic Toothfish (Dissostichus Mawsoni) Fishery?” Antarctic Science 26, no. 1: 3–14.
Alfaro, M. E., D. I. Bolnick, and P. C. Wainwright. 2005. “Evolutionary Consequences of Many-To-One Mapping of Jaw Morphology to Mechanics in Labrid Fishes.” American Naturalist 165, no. 6: E140–E154.
Balguerias, E. 2000. “Changes in Biomass of Eight Species of Finfish Around the South Orkney Islands (Subarea 48.2) From Three Bottom Trawl Surveys.” CCAMLR Science 7: 53–74.
Benjamini, Y., and Y. Hochberg. 1995. “Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing.” Journal of the Royal Statistical Society 57, no. 1: 289–300.
Berner, D. 2011. “Size Correction in Biology: How Reliable Are Approaches Based on (Common) Principal Component Analysis?” Oecologia 166, no. 4: 961–971.
Bista, I., J. M. D. Wood, T. Desvignes, et al. 2023. “Genomics of Cold Adaptations in the Antarctic Notothenioid Fish Radiation.” Nature Communications 14, no. 1: 3412.
Blin, M., L. Valay, M. Kuratko, M. Pavie, and S. Rétaux. 2024. “The Evolution of Olfactory Sensitivity, Preferences, and Behavioral Responses in Mexican Cavefish Is Influenced by Fish Personality.” eLife 12: RP92861. https://doi.org/10.7554/elife.92861.3.
Blomberg, S. P., T. Garland Jr., and A. R. Ives. 2003. “Testing for Phylogenetic Signal in Comparative Data: Behavioral Traits Are More Labile.” Evolution 57, no. 4: 717–745.
Bowmaker, J. K. 2008. “Evolution of Vertebrate Visual Pigments.” Vision Research 48, no. 20: 2022–2041.
Brown, A., and S. Thatje. 2014. “Explaining Bathymetric Diversity Patterns in Marine Benthic Invertebrates and Demersal Fishes: Physiological Contributions to Adaptation of Life at Depth.” Biological Reviews of the Cambridge Philosophical Society 89, no. 2: 406–426.
Brownstein, C. D., A. Dornburg, and T. J. Near. 2024. “Cenozoic Evolutionary History Obscures the Mesozoic Origins of Acanthopterygian Fishes.” In bioRxiv. https://doi.org/10.1101/2024.09.30.615987.
Brownstein, C. D., K. L. Zapfe, S. Lott, et al. 2024. “Reproductive Innovation Enabled Radiation in the Deep Sea During an Ecological Crisis.” In bioRxiv. https://doi.org/10.1101/2024.01.12.575380.
Burton, R. F. 2008. “The Scaling of Eye Size in Adult Birds: Relationship to Brain, Head and Body Sizes.” Vision Research 48, no. 22: 2345–2351.
Casaux, R., M. L. Bertolin, and A. Carlini. 2011. “Feeding Habits of Three Seal Species at the Danco Coast, Antarctica: A Re-Assessment.” Polar Biology 34, no. 10: 1615–1620.
Caves, E. M., T. T. Sutton, and S. Johnsen. 2017. “Visual Acuity in Ray-Finned Fishes Correlates With Eye Size and Habitat.” Journal of Experimental Biology 220, no. Pt 9: 1586–1596.
Chen, J.-N., S. Samadi, and W.-J. Chen. 2018. “Rhodopsin Gene Evolution in Early Teleost Fishes.” PLoS One 13, no. 11: e0206918.
Chen, L., Y. Lu, W. Li, et al. 2019. “The Genomic Basis for Colonizing the Freezing Southern Ocean Revealed by Antarctic Toothfish and Patagonian Robalo Genomes.” GigaScience 8, no. 4: giz016. https://doi.org/10.1093/gigascience/giz016.
Chinen, A., T. Hamaoka, Y. Yamada, and S. Kawamura. 2003. “Gene Duplication and Spectral Diversification of Cone Visual Pigments of Zebrafish.” Genetics 163, no. 2: 663–675.
Constable, A. J., W. K. de la Mare, D. J. Agnew, I. Everson, and D. Miller. 2000. “Managing Fisheries to Conserve the Antarctic Marine Ecosystem: Practical Implementation of the Convention on the Conservation of Antarctic Marine Living Resources (CCAMLR).” ICES Journal of Marine Science 57, no. 3: 778–791.
Corral-López, A., M. Garate-Olaizola, S. D. Buechel, N. Kolm, and A. Kotrschal. 2017. “On the Role of Body Size, Brain Size, and Eye Size in Visual Acuity.” Behavioral Ecology and Sociobiology 71, no. 12: 179.
Costello, M. J., and C. Chaudhary. 2017. “Marine Biodiversity, Biogeography, Deep-Sea Gradients, and Conservation.” Current Biology 27, no. 13: 2051.
Daane, J. M., A. Dornburg, P. Smits, et al. 2019. “Historical Contingency Shapes Adaptive Radiation in Antarctic Fishes.” Nature Ecology & Evolution 3, no. 7: 1102–1109.
Daane, J. M., A. Dornburg, P. Smits, et al. 2020. “Author Correction: Historical Contingency Shapes Adaptive Radiation in Antarctic Fishes.” Nature Ecology & Evolution 4, no. 4: 659.
Daane, J. M., and H. William Detrich III. 2021. “Adaptations and Diversity of Antarctic Fishes: A Genomic Perspective.” Annual Review of Animal Biosciences 10: 39–62. https://doi.org/10.1146/annurev-animal-081221-064325.
Daniels, R. A. 1982. “Feeding Ecology of Some Fishes of the Antarctic Peninsula”.
de Busserolles, F., J. L. Fitzpatrick, N. J. Marshall, and S. P. Collin. 2014. “The Influence of Photoreceptor Size and Distribution on Optical Sensitivity in the Eyes of Lanternfishes (Myctophidae).” PLoS One 9, no. 6: e99957.
de Busserolles, F., J. L. Fitzpatrick, J. R. Paxton, N. Justin Marshall, and S. P. Collin. 2013. “Eye-Size Variability in Deep-Sea Lanternfishes (Myctophidae): An Ecological and Phylogenetic Study.” PLoS One 8, no. 3: e58519.
de Busserolles, F., L. Fogg, F. Cortesi, and J. Marshall. 2020. “The Exceptional Diversity of Visual Adaptations in Deep-Sea Teleost Fishes.” Seminars in Cell & Developmental Biology 106: 20–30.
de Busserolles, F., and N. J. Marshall. 2017. “Seeing in the Deep-Sea: Visual Adaptations in Lanternfishes.” Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 372, no. 1717: 20160070. https://doi.org/10.1098/rstb.2016.0070.
Dornburg, A., S. Federman, A. D. Lamb, C. D. Jones, and T. J. Near. 2017. “Cradles and Museums of Antarctic Teleost Biodiversity.” Nature Ecology & Evolution 1, no. 9: 1379–1384.
Eastman, J. T. 1985. “Pleuragramma Antarcticum (Pisces, Nototheniidae) as Food for Other Fishes in McMurdo Sound, Antarctica.” Polar Biology 4, no. 3: 155–160. https://doi.org/10.1007/BF00263878.
Eastman, J. T. 2000. “Antarctic Notothenioid Fishes as Subjects for Research in Evolutionary Biology.” Antarctic Science 12, no. 3: 276–287. https://doi.org/10.1017/s0954102000000341.
Eastman, J. T. 2017. “Bathymetric Distributions of Notothenioid Fishes.” Polar Biology 40, no. 10: 2077–2095.
Eastman, J. T. 2020. “The Buoyancy-Based Biotope Axis of the Evolutionary Radiation of Antarctic Cryonotothenioid Fishes.” Polar Biology 43, no. 9: 1217–1231.
Eastman, J. T., and R. R. Eakin. 2021. “Checklist of the species of notothenioid fishes.” Antarctic Science 33, no. 3: 273–280. https://doi.org/10.1017/S0954102020000632.
Eastman, J. T., and A. L. DeVries. 1982. “Buoyancy Studies of Notothenioid Fishes in McMurdo Sound, Antarctica.” Copeia 1982, no. 2: 385. https://doi.org/10.2307/1444619.
Eastman, J. T., and A. R. McCune. 2000. “Fishes on the Antarctic Continental Shelf: Evolution of a Marine Species Flock?” Journal of Fish Biology 57: 84–102.
Eddy, S. R. 2009. “A New Generation of Homology Search Tools Based on Probabilistic Inference.” Genome Informatics 23, no. 1: 205–211.
Edmunds, N. B., K. S. McCann, and F. Laberge. 2016. “Food Web Structure Shapes the Morphology of Teleost Fish Brains.” Brain, Behavior and Evolution 87, no. 2: 128–138.
Foster, K. L., T. Garland Jr., L. Schmitz, and T. E. Higham. 2018. “Skink Ecomorphology: Forelimb and Hind Limb Lengths, but Not Static Stability, Correlate With Habitat Use and Demonstrate Multiple Solutions.” Biological Journal of the Linnean Society 125: 673–692. https://doi.org/10.1093/biolinnean/bly146.
Fujiyabu, C., K. Sato, N. M. L. Utari, H. Ohuchi, Y. Shichida, and T. Yamashita. 2019. “Evolutionary History of Teleost Intron-Containing and Intron-Less Rhodopsin Genes.” Scientific Reports 9, no. 1: 10653.
Fukunaga, A., R. K. Kosaki, D. Wagner, and C. Kane. 2016. “Structure of Mesophotic Reef Fish Assemblages in the Northwestern Hawaiian Islands.” PLoS One 11, no. 7: e0157861.
Gavrilets, S., and J. B. Losos. 2009. “Adaptive Radiation: Contrasting Theory With Data.” Science 323, no. 5915: 732–737.
Goatley, C. H. R., and D. R. Bellwood. 2009. “Morphological Structure in a Reef Fish Assemblage.” Coral Reefs 28, no. 2: 449–457.
Guthrie, S. D. M. 1990. “The Physiology of the Teleostean Optic Tectum.” In The Visual System of Fish, edited by R. Douglas, and M. Djamgoz, 279–343. Springer Netherlands, Dordrecht.
Hamaoka, T., M. Takechi, A. Chinen, Y. Nishiwaki, and S. Kawamura. 2002. “Visualization of Rod Photoreceptor Development Using GFP-Transgenic Zebrafish.” Genesis 34, no. 3: 215–220.
Harmon, L. J., J. A. Schulte II, A. Larson, and J. B. Losos. 2003. “Tempo and Mode of Evolutionary Radiation in Iguanian Lizards.” Science 301, no. 5635: 961–964.
Howell, K. J., S. M. Beston, S. Stearns, and M. R. Walsh. 2021. “Coordinated Evolution of Brain Size, Structure, and Eye Size in Trinidadian Killifish.” Ecology and Evolution 11, no. 1: 365–375.
Huber, R., M. J. van Staaden, L. S. Kaufman, and K. F. Liem. 1997. “Microhabitat Use, Trophic Patterns, and the Evolution of Brain Structure in African Cichlids.” Brain, Behavior and Evolution 50, no. 3: 167–182.
Hunt, D. E., N. J. F. Rawlinson, G. A. Thomas, and J. M. Cobcroft. 2015. “Investigating Photoreceptor Densities, Potential Visual Acuity, and Cone Mosaics of Shallow Water, Temperate Fish Species.” Vision Research 111: 13–21.
Hunt, D. M., K. S. Dulai, J. C. Partridge, P. Cottrill, and J. K. Bowmaker. 2001. “The Molecular Basis for Spectral Tuning of Rod Visual Pigments in Deep-Sea Fish.” Journal of Experimental Biology 204, no. Pt 19: 3333–3344.
Iglesias, T. L., A. Dornburg, D. L. Warren, P. C. Wainwright, L. Schmitz, and E. P. Economo. 2018. “Eyes Wide Shut: The Impact of Dim-Light Vision on Neural Investment in Marine Teleosts.” Journal of Evolutionary Biology 31, no. 8: 1082–1092.
Ingram, T. 2011. “Speciation Along a Depth Gradient in a Marine Adaptive Radiation.” Proceedings of the Royal Society B: Biological Sciences 278, no. 1705: 613–618. https://doi.org/10.1098/rspb.2010.1127.
John, C. A. S., C. A. St. John, T. J. Buser, et al. 2022. “Diversification Along a Benthic to Pelagic Gradient Contributes to Fish Diversity in the World's Largest Lake (Lake Baikal, Russia).” Molecular Ecology 31, no. 1: 238–251. https://doi.org/10.1111/mec.16209.
Jones, C. D., M. Damerau, K. Deitrich, et al. 2009. “Demersal Finfish Survey of the South Orkney Islands.” NOAA Technical Memorandum NMFS SWFSC 445: 49–66.
Jones, C. D., and T. J. Near. 2012. “The Reproductive Behaviour of Pogonophryne Scotti Confirms Widespread Egg-Guarding Parental Care Among Antarctic Notothenioids.” Journal of Fish Biology 80, no. 7: 2629–2635.
Katoh, K. 2002. “MAFFT: A Novel Method for Rapid Multiple Sequence Alignment Based on Fast Fourier Transform.” Nucleic Acids Research 30, no. 14: 3059–3066. https://doi.org/10.1093/nar/gkf436.
Khabbazian, M., R. Kriebel, K. Rohe, and C. Ané. 2016. “Fast and Accurate Detection of Evolutionary Shifts in Ornstein–Uhlenbeck Models.” Methods in Ecology and Evolution 7, no. 7: 811–824.
Kotrschal, A., A. E. Deacon, A. E. Magurran, and N. Kolm. 2017. “Predation Pressure Shapes Brain Anatomy in the Wild.” Evolutionary Ecology 31, no. 5: 619–633.
Kröger, R. H. H., K. A. Fritsches, and E. J. Warrant. 2009. “Lens Optical Properties in the Eyes of Large Marine Predatory Teleosts.” Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 195, no. 2: 175–182.
Kuball, K., V. F. L. Fernandes, D. Takagi, and M. Yoshizawa. 2024. “Blind Cavefish Evolved Higher Foraging Responses to Chemo- and Mechanostimuli.” PLoS One 19, no. 5: e0300793.
La Mesa, M., M. Dalú, and M. Vacchi. 2004. “Trophic Ecology of the Emerald Notothen Trematomus Bernacchii (Pisces, Nototheniidae) From Terra Nova Bay, Ross Sea, Antarctica.” Polar Biology 27, no. 11: 721–728.
La Mesa, M., J. T. Eastman, and M. Vacchi. 2004. “The Role of Notothenioid Fish in the Food Web of the Ross Sea Shelf Waters: A Review.” Polar Biology 27, no. 6: 321–338.
La Mesa, M., F. Llompart, E. Riginella, and J. T. Eastman. 2021. “Parental Care and Reproductive Strategies in Notothenioid Fishes.” Fish and Fisheries 22, no. 2: 356–376.
Larsson, A. 2014. “AliView: A Fast and Lightweight Alignment Viewer and Editor for Large Datasets.” Bioinformatics 30, no. 22: 3276–3278. https://doi.org/10.1093/bioinformatics/btu531.
Lin, J.-J., F.-Y. Wang, W.-H. Li, and T.-Y. Wang. 2017. “The Rises and Falls of Opsin Genes in 59 Ray-Finned Fish Genomes and Their Implications for Environmental Adaptation.” Scientific Reports 7, no. 1: 15568.
Lythgoe, J. N., W. R. A. Muntz, J. C. Partridge, J. Shand, and D. Williams. 1994. “The Ecology of the Visual Pigments of Snappers (Lutjanidae) on the Great Barrier Reef.” Journal of Comparative Physiology A 174, no. 4: 461–467. https://doi.org/10.1007/bf00191712.
MacIver, M. A., L. Schmitz, U. Mugan, T. D. Murphey, and C. D. Mobley. 2017. “Massive Increase in Visual Range Preceded the Origin of Terrestrial Vertebrates.” Proceedings of the National Academy of Sciences of the United States of America 114, no. 12: E2375–E2384.
Marranzino, A. N., and J. F. Webb. 2018. “Flow Sensing in the Deep Sea: The Lateral Line System of Stomiiform Fishes.” Zoological Journal of the Linnean Society 183, no. 4: 945–965.
Marshall, J., K. L. Carleton, and T. Cronin. 2015. “Colour Vision in Marine Organisms.” Current Opinion in Neurobiology 34: 86–94.
Matschiner, M., R. Hanel, and W. Salzburger. 2011. “On the Origin and Trigger of the Notothenioid Adaptive Radiation.” PLoS One 6, no. 4: e18911.
Minh, B. Q., C. C. Dang, L. S. Vinh, and R. Lanfear. 2021. “QMaker: Fast and Accurate Method to Estimate Empirical Models of Protein Evolution.” Systematic Biology 70, no. 5: 1046–1060.
Minh, B. Q., H. A. Schmidt, O. Chernomor, et al. 2020. “IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era.” Molecular Biology and Evolution 37, no. 5: 1530–1534.
Miyazaki, T., and T. Iwami. 2012. “Molecular Cloning of cDNA Encoding Red Opsin Gene in the Retinas of Five Antarctic Notothenioid Fishes.” Polar Biology 35, no. 5: 775–783.
Modica, M. V., J. Gorson, A. E. Fedosov, et al. 2020. “Macroevolutionary Analyses Suggest That Environmental Factors, Not Venom Apparatus, Play Key Role in Terebridae Marine Snail Diversification.” Systematic Biology 69, no. 3: 413–430. https://doi.org/10.1093/sysbio/syz059.
Montgomery, J. C., and J. A. Macdonald. 1998. “Evolution of Sensory Systems: A Comparison of Antarctic and Deep-Sea Ichthyofauna.” In Fishes of Antarctica, edited by J. A. Macdonald, 329–338. Milan: Springer.
Moore, B. R., S. Höhna, M. R. May, B. Rannala, and J. P. Huelsenbeck. 2016. “Critically Evaluating the Theory and Performance of Bayesian Analysis of Macroevolutionary Mixtures.” Proceedings of the National Academy of Sciences of the United States of America 113, no. 34: 9569–9574.
Morrow, J. M., S. Lazic, and B. S. W. Chang. 2011. “A Novel Rhodopsin-Like Gene Expressed in Zebrafish Retina.” Visual Neuroscience 28, no. 4: 325–335.
Morrow, J. M., S. Lazic, M. Dixon Fox, et al. 2017. “A Second Visual Rhodopsin Gene, rh1-2, Is Expressed in Zebrafish Photoreceptors and Found in Other Ray-Finned Fishes.” Journal of Experimental Biology 220, no. Pt 2: 294–303.
Musilova, Z., W. Salzburger, and F. Cortesi. 2021. “The Visual Opsin Gene Repertoires of Teleost Fishes: Evolution, Ecology, and Function.” Annual Review of Cell and Developmental Biology 37: 441–468.
Near, T. J., A. Dornburg, K. L. Kuhn, et al. 2012. “Ancient Climate Change, Antifreeze, and the Evolutionary Diversification of Antarctic Fishes.” Proceedings of the National Academy of Sciences of the United States of America 109, no. 9: 3434–3439.
Near, T. J., B. J. Kendrick, W. H. Detrich III, and C. D. Jones. 2007. “Confirmation of Neutral Buoyancy in Aethotaxis Mitopteryx DeWitt (Notothenioidei: Nototheniidae).” Polar Biology 30, no. 4: 443–447.
Near, T. J., S. E. Russo, C. D. Jones, and A. L. DeVries. 2003. “Ontogenetic Shift in Buoyancy and Habitat in the Antarctic Toothfish, Dissostichus Mawsoni (Perciformes: Nototheniidae).” Polar Biology 26, no. 2: 124–128. https://doi.org/10.1007/s00300-002-0459-7.
Near, T. J., D. J. MacGuigan, E. Parker, C. D. Struthers, C. D. Jones, and A. Dornburg. 2018. “Phylogenetic Analysis of Antarctic Notothenioids Illuminates the Utility of RADseq for Resolving Cenozoic Adaptive Radiations.” Molecular phylogenetics and evolution 129, 268–279.
Nilsson, D.-E., E. J. Warrant, S. Johnsen, R. Hanlon, and N. Shashar. 2012. “A Unique Advantage for Giant Eyes in Giant Squid.” Current Biology 22, no. 8: 683–688.
Pagel, M. 1999. “Inferring the Historical Patterns of Biological Evolution.” Nature 401, no. 6756: 877–884.
Paradis, E., J. Claude, and K. Strimmer. 2004. “APE: Analyses of Phylogenetics and Evolution in R Language.” Bioinformatics 20, no. 2: 289–290.
Parker, E., K. L. Zapfe, J. Yadav, et al. 2022. “Periodic Environmental Disturbance Drives Repeated Ecomorphological Diversification in an Adaptive Radiation of Antarctic Fishes.” American Naturalist 200, no. 6: E221–E236. https://doi.org/10.1086/721373.
Patarnello, T., C. Verde, G. di Prisco, L. Bargelloni, and L. Zane. 2011. “How Will Fish That Evolved at Constant Sub-Zero Temperatures Cope With Global Warming? Notothenioids as a Case Study.” BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology 33, no. 4: 260–268.
Pennell, M. W., J. M. Eastman, G. J. Slater, et al. 2014. “Geiger v2.0: An Expanded Suite of Methods for Fitting Macroevolutionary Models to Phylogenetic Trees.” Bioinformatics 30, no. 15: 2216–2218.
Pinheiro, J., and D. M. Bates. 2000. Mixed-Effects Models in S and S-PLUS. 1st ed. New York, NY: Springer.
Pisani, D., S. M. Mohun, S. R. Harris, J. O. McInerney, and M. Wilkinson. 2006. “Molecular Evidence for Dim-Light Vision in the Last Common Ancestor of the Vertebrates.” Current Biology 16, no. 9: R318–R319. https://doi.org/10.1016/j.cub.2006.03.090.
Pointer, M. A., C.-H. C. Cheng, J. K. Bowmaker, et al. 2005. “Adaptations to an Extreme Environment: Retinal Organisation and Spectral Properties of Photoreceptors in Antarctic Notothenioid Fish.” Journal of Experimental Biology 208, no. Pt 12: 2363–2376.
Purser, A., L. Hehemann, L. Boehringer, et al. 2022. “A Vast Icefish Breeding Colony Discovered in the Antarctic.” Current Biology 32, no. 4: 842–850.e4.
Puttick, M. N., T. Ingram, M. Clarke, and G. H. Thomas. 2020. “MOTMOT: Models of Trait Macroevolution on Trees (An Update).” Methods in Ecology and Evolution 11, no. 3: 464–471.
Quang, L. S., O. Gascuel, and N. Lartillot. 2008. “Empirical Profile Mixture Models for Phylogenetic Reconstruction.” Bioinformatics 24, no. 20: 2317–2323.
Rabosky, D. L. 2014. “Automatic Detection of Key Innovations, Rate Shifts, and Diversity-Dependence on Phylogenetic Trees.” PLoS One 9, no. 2: e89543.
Rabosky, D. L., M. Grundler, C. Anderson, et al. 2014. “BAMMtools: An R Package for the Analysis of Evolutionary Dynamics on Phylogenetic Trees.” Methods in Ecology and Evolution 5, no. 7: 701–707.
Rabosky, D. L., J. S. Mitchell, and J. Chang. 2017. “Is BAMM Flawed? Theoretical and Practical Concerns in the Analysis of Multi-Rate Diversification Models.” Systematic Biology 66, no. 4: 477–498. https://doi.org/10.1093/sysbio/syx037.
Rennison, D. J., G. L. Owens, and J. S. Taylor. 2012. “Opsin Gene Duplication and Divergence in Ray-Finned Fish.” Molecular Phylogenetics and Evolution 62, no. 3: 986–1008.
Revell, L. J. 2012. “Phytools: An R Package for Phylogenetic Comparative Biology (and Other Things).” Methods in Ecology and Evolution 3, no. 2: 217–223.
Ricci, V., F. Ronco, N. Boileau, and W. Salzburger. 2023. “Visual Opsin Gene Expression Evolution in the Adaptive Radiation of Cichlid Fishes of Lake Tanganyika.” Science Advances 9, no. 36: eadg6568.
Ricci, V., F. Ronco, Z. Musilova, and W. Salzburger. 2022. “Molecular Evolution and Depth-Related Adaptations of Rhodopsin in the Adaptive Radiation of Cichlid Fishes in Lake Tanganyika.” Molecular Ecology 31, no. 10: 2882–2897.
Rohlf, F. J. 2006. tpsDig, Digitize Landmarks and Outlines, Version 2.05. Stony Brook, NY: Department of Ecology and Evolution, State University of New York.
Rosa, R., H. M. Dierssen, L. Gonzalez, and B. A. Seibel. 2008. “Large-Scale Diversity Patterns of Cephalopods in the Atlantic Open Ocean and Deep Sea.” Ecology 89, no. 12: 3449–3461.
Ruppé, L., G. Clément, A. Herrel, et al. 2015. “Environmental Constraints Drive the Partitioning of the Soundscape in Fishes.” Proceedings of the National Academy of Sciences of the United States of America 112, no. 19: 6092–6097.
Rutschmann, S., M. Matschiner, M. Damerau, et al. 2011. “Parallel Ecological Diversification in Antarctic Notothenioid Fishes as Evidence for Adaptive Radiation.” Molecular Ecology 20, no. 22: 4707–4721.
Schmitz, L., and P. C. Wainwright. 2011. “Nocturnality Constrains Morphological and Functional Diversity in the Eyes of Reef Fishes.” BMC Evolutionary Biology 11: 338.
Simpson, G. G. 1953. The Major Features of Evolution. New York: Columbia University Press.
Slater, G. J. 2013. “Phylogenetic Evidence for a Shift in the Mode of Mammalian Body Size Evolution at the Cretaceous-Palaeogene Boundary.” Methods in Ecology and Evolution 4, no. 8: 734–744.
Smith, K. F., and J. H. Brown. 2002. “Patterns of Diversity, Depth Range and Body Size Among Pelagic Fishes Along a Gradient of Depth.” Global Ecology and Biogeography 11, no. 4: 313–322. https://doi.org/10.1046/j.1466-822x.2002.00286.x.
Strugnell, J. M., P. C. Watts, P. J. Smith, and A. L. Allcock. 2012. “Persistent Genetic Signatures of Historic Climatic Events in an Antarctic Octopus.” Molecular Ecology 21, no. 11: 2775–2787.
Sugawara, T., Y. Terai, H. Imai, et al. 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, no. 15: 5448–5453.
Sutton, T. T. 2013. “Vertical Ecology of the Pelagic Ocean: Classical Patterns and New Perspectives.” Journal of Fish Biology 83, no. 6: 1508–1527.
Takenaka, N., and S. Yokoyama. 2007. “Mechanisms of Spectral Tuning in the RH2 Pigments of Tokay Gecko and American Chameleon.” Gene 399, no. 1: 26–32.
Terakita, A. 2005. “The Opsins.” Genome Biology 6, no. 3: 1–9.
Thatje, S., C.-D. Hillenbrand, and R. Larter. 2005. “On the Origin of Antarctic Marine Benthic Community Structure.” Trends in Ecology & Evolution 20, no. 10: 534–540.
Thatje, S., C.-D. Hillenbrand, A. Mackensen, and R. Larter. 2008. “Life Hung by a Thread: Endurance of Antarctic Fauna in Glacial Periods.” Ecology 89, no. 3: 682–692.
Tilzer, M. M., W. W. Gieskes, R. Heusel, and N. Fenton. 1994. “The Impact of Phytoplankton on Spectral Water Transparency in the Southern Ocean: Implications for Primary Productivity.” Polar Biology 14, no. 2: 124–136. https://doi.org/10.1007/bf00234975.
Vacchi, M., E. Pisano, and L. Ghigliotti. 2017. The Antarctic Silverfish: A Keystone Species in a Changing Ecosystem. Berlin: Springer.
Vinterstare, J., K. Hulthén, D. E. Nilsson, P. A. Nilsson, and C. Brönmark. 2020. “More Than Meets the Eye: Predator-Induced Pupil Size Plasticity in a Teleost Fish.” Journal of Animal Ecology 89, no. 10: 2258–2267. https://doi.org/10.1111/1365-2656.13303.
Wagner, H. J., E. Fröhlich, K. Negishi, and S. P. Collin. 1998. “The Eyes of Deep-Sea Fish. II. Functional Morphology of the Retina.” Progress in Retinal and Eye Research 17, no. 4: 637–685.
Wainwright, P. C., M. E. Alfaro, D. I. Bolnick, and C. D. Hulsey. 2005. “Many-To-One Mapping of Form to Function: A General Principle in Organismal Design?” Integrative and Comparative Biology 45, no. 2: 256–262.
Warrant, E. 2000. “The Eyes of Deep-Sea Fishes and the Changing Nature of Visual Scenes With Depth.” Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 355, no. 1401: 1155–1159.
Warrant, E. 2004. “Vision in the Dimmest Habitats on Earth.” Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 190, no. 10: 765–789.
Warrant, E. J., S. P. Collin, and N. A. Locket. 2008. “Eye Design and Vision in Deep-Sea Fishes.” In Sensory Processing in Aquatic Environments, edited by S. P. Collin, 303–322. New York, NY: Springer.
Warrant, E. J., and N. A. Locket. 2004. “Vision in the Deep Sea.” Biological Reviews of the Cambridge Philosophical Society 79, no. 3: 671–712.
White, G. E., and C. Brown. 2015. “Microhabitat Use Affects Brain Size and Structure in Intertidal Gobies.” Brain, Behavior and Evolution 85, no. 2: 107–116.
Yamamoto, N. 2017. “Adaptive Radiation and Vertebrate Brain Diversity: Cases of Teleosts.” In Diversity and Commonality in Animals, 253–271. Tokyo: Springer Japan.
Yokoyama, S. 2002. “Molecular Evolution of Color Vision in Vertebrates.” Gene 300, no. 1–2: 69–78. https://doi.org/10.1016/s0378-1119(02)00845-4.
Yokoyama, S. 2008. “Evolution of Dim-Light and Color Vision Pigments.” Annual Review of Genomics and Human Genetics 9: 259–282.
Yokoyama, S., and H. Jia. 2020. “Origin and Adaptation of Green-Sensitive (RH2) Pigments in Vertebrates.” FEBS Open Bio 10, no. 5: 873–882.
Yokoyama, S., T. Tada, H. Zhang, and L. Britt. 2008. “Elucidation of Phenotypic Adaptations: Molecular Analyses of Dim-Light Vision Proteins in Vertebrates.” Proceedings of the National Academy of Sciences of the United States of America 105, no. 36: 13480–13485.
Yokoyama, S., N. Takenaka, and N. Blow. 2007. “A Novel Spectral Tuning in the Short Wavelength-Sensitive (SWS1 and SWS2) Pigments of Bluefin Killifish (Lucania Goodei).” Gene 396, no. 1: 196–202.
Yokoyama, S., H. Zhang, F. B. Radlwimmer, and N. S. Blow. 1999. “Adaptive Evolution of Color Vision of the Comoran Coelacanth (Latimeria Chalumnae).” Proceedings of the National Academy of Sciences of the United States of America 96, no. 11: 6279–6284.
