Massive increase in visual range preceded the origin of terrestrial vertebrates
Edited by Neil H. Shubin, The University of Chicago, Chicago, IL, and approved January 24, 2017 (received for review September 17, 2016)
Science Sessions podcast
June 11, 2019
Significance
Starting 385 million years ago, certain fish slowly evolved into legged animals living on land. We show that eyes tripled in size and shifted from the sides to the top of the head long before fish modified their fins into limbs for land. Before permanent life on land, these animals probably hunted like crocodiles, looking at prey from just above the water line, where the vastly higher transparency of air enabled long-distance vision and selected for larger eyes. The “buena vista” hypothesis that our study forwards is that seeing opportunities far away provided an informational zip line to the bounty of invertebrate prey on land, aiding selection for limbs—first for brief forays onto land and eventually, for life there.
Abstract
The evolution of terrestrial vertebrates, starting around 385 million years ago, is an iconic moment in evolution that brings to mind images of fish transforming into four-legged animals. Here, we show that this radical change in body shape was preceded by an equally dramatic change in sensory abilities akin to transitioning from seeing over short distances in a dense fog to seeing over long distances on a clear day. Measurements of eye sockets and simulations of their evolution show that eyes nearly tripled in size just before vertebrates began living on land. Computational simulations of these animal’s visual ecology show that for viewing objects through water, the increase in eye size provided a negligible increase in performance. However, when viewing objects through air, the increase in eye size provided a large increase in performance. The jump in eye size was, therefore, unlikely to have arisen for seeing through water and instead points to an unexpected hybrid of seeing through air while still primarily inhabiting water. Our results and several anatomical innovations arising at the same time suggest lifestyle similarity to crocodiles. The consequent combination of the increase in eye size and vision through air would have conferred a 1 million-fold increase in the amount of space within which objects could be seen. The “buena vista” hypothesis that our data suggest is that seeing opportunities from afar played a role in the subsequent evolution of fully terrestrial limbs as well as the emergence of elaborated action sequences through planning circuits in the nervous system.
Data Availability
Data deposition: Code and data to reproduce these results is available at https://doi.org/10.5281/zenodo.321923.
Acknowledgments
We thank Scott Schaper and Olivia Carmo for assistance with data collection and Ian Abraham for coding the ball control example (SI Appendix, Fig. S8). We also thank Josef Uyeda for assistance with the bayou package. The image of Eusthenopteron is courtesy of John Merck (University of Maryland), and reconstruction of Acanthostega is courtesy of Michael Coates (University of Chicago). We thank Sönke Johnsen (Duke University) for providing the starlight spectra used in this study. Marco Gallio, Michael Paulin, and Peter C. Wainwright gave valuable feedback on an earlier draft. This work was partially funded by National Science Foundation Grants IOS-ORG 1456830 (to M.A.M.) and PECASE IOB-0846032 (to M.A.M.), and the support of Northwestern University during M.A.M.’s 3-mo academic leave.
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Freely available online through the PNAS open access option.
Data Availability
Data deposition: Code and data to reproduce these results is available at https://doi.org/10.5281/zenodo.321923.
Submission history
Published online: March 7, 2017
Published in issue: March 21, 2017
Keywords
Acknowledgments
We thank Scott Schaper and Olivia Carmo for assistance with data collection and Ian Abraham for coding the ball control example (SI Appendix, Fig. S8). We also thank Josef Uyeda for assistance with the bayou package. The image of Eusthenopteron is courtesy of John Merck (University of Maryland), and reconstruction of Acanthostega is courtesy of Michael Coates (University of Chicago). We thank Sönke Johnsen (Duke University) for providing the starlight spectra used in this study. Marco Gallio, Michael Paulin, and Peter C. Wainwright gave valuable feedback on an earlier draft. This work was partially funded by National Science Foundation Grants IOS-ORG 1456830 (to M.A.M.) and PECASE IOB-0846032 (to M.A.M.), and the support of Northwestern University during M.A.M.’s 3-mo academic leave.
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This article is a PNAS Direct Submission.
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The authors declare no conflict of interest.
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Massive increase in visual range preceded the origin of terrestrial vertebrates, Proc. Natl. Acad. Sci. U.S.A.
114 (12) E2375-E2384,
https://doi.org/10.1073/pnas.1615563114
(2017).
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