Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-848d4c4894-75dct Total loading time: 0 Render date: 2024-04-30T10:53:24.731Z Has data issue: false hasContentIssue false

1 - The Evolution of Eyes

Published online by Cambridge University Press:  17 September 2021

By
Dan-Eric Nilsson
Edited by
Andrew Fabian ,
Janet Gibson ,
Mike Sheppard  and
Simone Weyand
With contributions by
Andrew Blake ,
Carolin Crawford ,
Paul Fletcher ,
Sophie Hackford ,
Anya Hurlbert ,
Dan-Eric Nilsson  and
Carlo Rovelli
Andrew Fabian
Affiliation:
University of Cambridge
Janet Gibson
Affiliation:
Darwin College, Cambridge
Mike Sheppard
Affiliation:
University of Cambridge
Simone Weyand
Affiliation:
University of Cambridge
Andrew Blake
Affiliation:
Samsung AI Research Centre
Carolin Crawford
Affiliation:
University of Cambridge
Paul Fletcher
Affiliation:
University of Cambridge
Sophie Hackford
Affiliation:
Wired Magazine
Anya Hurlbert
Affiliation:
Newcastle University
Dan-Eric Nilsson
Affiliation:
Lunds Universitet, Sweden
Carlo Rovelli
Affiliation:
International Centre for Theoretical Physics
Get access

Summary

Eyes abound in the animal kingdom. Some are large as basketballs and others are just fractions of a millimetre. Eyes also come in many different types, such as the compound eyes of insects, the mirror eyes of scallops or our own camera-like eyes. Common to all animal eyes is that they serve the same fundamental role of collecting external information for guiding the animal’s behaviour. But behaviours vary tremendously across the animal kingdom, and it turns out this is the key to understanding how eyes evolved. In the lecture we will take a tour from the first animals that could only sense the presence of light, to those that saw the first crude image of the world and finally to animals that use acute vision for interacting with other animals. Amazingly, all these stages of eye evolution still exist in animals living today, and this is how we can unravel the evolution of behaviours that has been the driving force behind eye evolution.

Keywords

evolution eyesoriginal eyesphotoreceptorsciliaryrhabdomericopsinscephalopodsvertebratesinvertebrates
Type
Chapter
Information
Vision , pp. 5 - 32
Publisher: Cambridge University Press
Print publication year: 2021

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Lamb, T. D., Pugh, E. N. Jr, and Collin, S. P. The origin of the vertebrate eye. Evol. Edu. Outreach 2008; 1: 415–426. DOI https://doi.org/10.1007/s12052–008-0091-2Google Scholar
Nilsson, D.-E. Eye ancestry: Old genes for new eyes. Curr. Biol. 1996; 6: 39–42. DOI https://doi.org/10.1016/S0960–9822(02)00417-7Google Scholar
Nilsson, D.-E. Eye evolution: A question of genetic promiscuity. Curr. Opin. Neurobiol. 2004; 14: 407–414. DOI https://doi.org/10.1016/j.cub.2005.01.027CrossRefGoogle ScholarPubMed
Nilsson, D.-E. Photoreceptor evolution: Ancient siblings serve different tasks. Curr. Biol. 2005; 15: R94–R96. DOI https://doi.org/10.1016/j.cub.2005.01.027Google Scholar
Nilsson, D.-E. The evolution of eyes and visually guided behaviour. Phil. Trans. R. Soc. B 2009; 364: 2833–2847. DOI https://doi.org/10.1098/rstb.2009.0083Google Scholar
Fain, G. L., Hardie, R., and Laughlin, S. B. Phototransduction and the evolution of photoreceptors. Curr. Biol. 2010; 20: R114–R124. DOI https://doi.org/10.1016/j.cub.2009.12.006Google Scholar
Nilsson, D.-E. Eye evolution and its functional basis. Visual Neurosci. 2013; 30: 5–20. DOI https://doi.org/10.1017/S0952523813000035Google Scholar
Porter, M. L., Blasic, J. R., Bok, M. J., Cameron, E. G., Pringle, T. et al. Shedding new light on opsin evolution. Phil. Trans. R. Soc. B 2012; 279: 3–14. DOI https://doi.org/10.1098/rspb.2011.1819Google Scholar
Liegertova, M., Pergner, J., Kozmikova, I., Fabian, P., Pombinho, A. R. et al. Cubozoan genome illuminates functional diversification of opsins and photoreceptor evolution. Sci. Rep. 2015; 5: 11885. DOI https://doi.org/10.1038/srep11885Google Scholar
Ramirez, M. D., Pairett, A. N., Pankey, M. S., Serb, J. M., Speiser, D. I. et al. The last common ancestor of most bilaterian animals possessed at least nine opsins. Genome Biol. Evol. 2016; 8: 3640–3652. DOI https://doi.org/10.1093/gbe/evw248Google Scholar
Land, M. F., and Nilsson, D.-E. General purpose and special purpose visual systems. In Warrant, E. J., and Nilsson, D.-E, eds. Invertebrate Vision. Cambridge: Cambridge University Press, 2006; 167–210.Google Scholar
Land, M. F., and Nilsson, D.-E. Animal Eyes, 2nd ed. Oxford: Oxford University Press, 2012.Google Scholar
Cronin, T. W., Johnsen, S., Marshall, N. J., and Warrant, E. J. Visual Ecology. Princeton, NJ and Oxford: Princeton University Press, 2014.Google Scholar
Foster, R. G., and Hankins, M. W. Non-rod, non-cone photoreception in the vertebrates. Prog. Retin. Eye Res. 2002; 21: 507–527. DOI https://doi.org/10.1016/j.conb.2005.06.011Google Scholar
de Mendoza, A., Sebe-Pedros, A., and Ruiz-Trillo, I. The evolution of the GPCR signaling system in eukaryotes: Modularity, conservation, and the transition to metazoan multicellularity. Genome Biol. Evol. 2014; 6: 606–619. DOI https://doi.org/10.1093/gbe/evu038Google Scholar
Colley, N, J., and Nilsson, D.-E. Photoreception in phytoplankton. Integ. Comp. Biol. 2016; 56: 764–775. DOI https://doi.org/10.1093/icb/icw037Google Scholar
D’Aniello, S., Delroisse, J., Valero-Gracia, A., Lowe, E. K., Byrne, M., et al. Opsin evolution in the Ambulacraria. Mar. Genom. 2015; 24: 177–183. DOI https://doi.org/10.1016/j.margen.2015.10.001Google Scholar
Tosches, M. A., Bucher, D., Vopalensky, P., and Arendt, D. Melatonin signaling controls circadian swimming behavior in marine zooplankton. Cell 2014; 159: 46–57. DOI https://doi.org/10.1016/j.cell.2014.07.042CrossRefGoogle ScholarPubMed
Dohrmann, M., and Wörheide, G. Dating early animal evolution using phylogenomic data. Sci. Rep. 2017; 7: 3599. DOI https://doi.org/10.1038/s41598–017-03791-wGoogle Scholar
Randel, N., and Jekely, G. Phototaxis and the origin of visual eyes. Phil. Trans. R. Soc. B 2016; 371: 20150042. DOI https://doi.org/10.1098/rstb.2015.0042Google Scholar
Nilsson, D.-E., and Bok, M. J. Low-resolution vision – at the hub of eye evolution. Integ. Comp. Biol. 2017; 57: 1066–1070. DOI https://doi.org/10.1093/icb/icx120Google Scholar
Eakin, R. M. Structure in invertebrate photoreceptors. In Autrum, H., ed. Handbook of Sensory Physiology, vol. 7. Berlin: Springer, 1972; 625–684.Google Scholar
Arendt, D., Tessmar-Raible, K., Snyman, H., Dorresteijn, A. W., and Wittbrodt, J. Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science 2004; 306: 869–871. DOI https://doi.org/10.1126/science.1099955CrossRefGoogle Scholar
Vopalensky, P., and Kozmik, Z. Eye evolution: Common use and independent recruitment of genetic components. Phil. Trans. R. Soc. B 2009; 364: 2819–2832. DOI https://doi.org/10.1098/rstb.2009.0079Google Scholar
Picciani, N., Kerlin, J. R., Sierra, N., Swafford, A. J., Ramirez, M. D. et al. Prolific origination of eyes in Cnidaria with co-option of non-visual opsins. Curr. Biol. 2018; 28: 2413–2419. DOI https://doi.org/10.1016/j.cub.2018.05.055Google Scholar
Nilsson, D.-E., Gislén, L., Coates, M. M., Skogh, C., and Garm, A. Advanced optics in a jellyfish eye. Nature 2005; 435: 201–205. DOI https://doi.org/10.1038/nature03484Google Scholar
Garm, A., O’Connor, M., Parkefelt, L., and Nilsson, D.-E. Visually guided obstacle avoidance in the box jellyfish Tripedalia cystophora and Chiropsella bronzie. J. Exp. Biol. 2007; 210: 3616–3623. DOI https://doi.org/10.1242/jeb.004044Google Scholar
Garm, A., Oskarsson, M., and Nilsson, D.-E. Box jellyfish use terrestrial visual cues for navigation. Curr. Biol. 2011; 21: 798–803. DOI https://doi.org/10.1016/j.cub.2011.03.054Google Scholar
Garm, A., and Nilsson, D.-E. Visual navigation in starfish: First evidence for the use of vision and eyes in starfish. Proc. R. Soc. B 2014; 281: 1–8. DOI https://doi.org/10.1098/rspb.2013.3011Google Scholar
Kirwan, J. D., Graf, J., Smolka, J., Mayer, G., Henze, M. J., and Nilsson, D.-E. Low resolution vision in a velvet worm (Onychophora). J. Exp. Biol. 2018; 221: 175802. DOI https://doi.org/10.1242/jeb.175802CrossRefGoogle Scholar
Nilsson, D.-E., Warrant, E. J., Johnsen, S., Hanlon, R., and Shashar, N. A unique advantage for giant eyes in giant squid. Curr. Biol. 2012; 22: 1–6. DOI https://doi.org/10.1016/j.cub.2012.02.031Google Scholar
Wiederman, S. D., Shoemaker, P. A., and O’Carroll, D. C. A model for the detection of moving targets in visual clutter inspired by insect physiology. PLoS One 2008; 3: e2784. DOI https://doi.org/10.1371/journal.pone.0002784Google Scholar
Parker, A. In the Blink of an Eye: The Cause of the Most Dramatic Event in the History of Life. London: Free Press, 2003.Google Scholar
Zhao, F., Bottjer, D. J., Hu, S., Yin, Z., and Zhu, M. Complexity and diversity of eyes in Early Cambrian ecosystems. Sci. Rep. 2013; 3: 2751. DOI https://doi.org/10.1038/srep02751Google Scholar
Nilsson, D.-E. Eyes as optical alarm systems in fan worms and ark clams. Philos. Trans. R. Soc. Biol. Sci. B 1994; 346: 195–212. DOI https://doi.org/10.1098/rstb.1994.0141Google Scholar
Bok, M. J., Capa, M., and Nilsson, D.-E. Here, there and everywhere: The radiolar eyes of fan worms (Annelida, Sabellidae). Integ. Comp. Biol. 2016; 56: 784–795. DOI https://doi.org/10.1093/icb/icw089Google Scholar
Bok, M. J., Porter, M. L., Ten Hove, H. A., Smith, R., and Nilsson, D.-E. Radiolar eyes of serpulid worms (Annelida, Serpulidae): Structures, function, and phototransduction. Biol. Bull. 2017; 233: 39–57. DOI https://doi.org/10.1086/694735Google Scholar
Gehring, W. J., and Ikeo, K. Pax 6: Mastering eye morphogenesis and eye evolution. Trends in Genetics 1999; 15, 371–377. DOI https://doi.org/10.1016/S0168-9525(99)01776-XGoogle Scholar
Nilsson, D.-E., and Arendt, D. Eye evolution: The blurry beginning. Curr. Biol. 2008; 18: R1096–R1098. DOI https://doi.org/10.1016/j.cub.2008.10.025Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×