A group of evolutionary biologists sees evidence for a hologenome. Others dismiss it
entirely. One thing’s certain: The debate remains heated.
Image credit: Shutterstock/Piriya Gutsch.
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Edited by Neil H. Shubin, The University of Chicago, Chicago, IL, and approved January 24, 2017 (received for review September 17, 2016)
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.
Footnotes
- ↵1To whom correspondence may be addressed. Email: maciver{at}northwestern.edu or lschmitz{at}kecksci.claremont.edu.
Author contributions: M.A.M. and L.S. designed research; M.A.M. and L.S. performed research; T.D.M. contributed new reagents/analytic tools; M.A.M., L.S., U.M., and C.D.M. analyzed data; and M.A.M. and L.S. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: Code and data to reproduce these results is available at https://doi.org/10.5281/zenodo.321923.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1615563114/-/DCSupplemental.
- Malcolm A. MacIvera,b,c,1,
- Lars Schmitzd,e,1,
- Ugurcan Muganc,
- Todd D. Murpheyb, and
- Curtis D. Mobleyf
- aThe Neuroscience and Robotics Laboratory, Northwestern University, Evanston, IL 60208;
- bDepartment of Mechanical Engineering, Northwestern University, Evanston, IL 60208;
- cDepartment of Biomedical Engineering, Northwestern University, Evanston, IL 60208;
- dW. M. Keck Science Department, Claremont McKenna, Pitzer, and Scripps Colleges, Claremont, CA 91711;
- eDinosaur Institute, Natural History Museum of Los Angeles County, Los Angeles, CA 90007;
- fSection for Optical Oceanography, Sequoia Scientific, Inc., Bellevue, WA 98005
Edited by Neil H. Shubin, The University of Chicago, Chicago, IL, and approved January 24, 2017 (received for review September 17, 2016)
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.
- fish–tetrapod transition
- vision
- visual ecology
- terrestriality
- prospective cognition
Footnotes
- ↵1To whom correspondence may be addressed. Email: maciver{at}northwestern.edu or lschmitz{at}kecksci.claremont.edu.
Author contributions: M.A.M. and L.S. designed research; M.A.M. and L.S. performed research; T.D.M. contributed new reagents/analytic tools; M.A.M., L.S., U.M., and C.D.M. analyzed data; and M.A.M. and L.S. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: Code and data to reproduce these results is available at https://doi.org/10.5281/zenodo.321923.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1615563114/-/DCSupplemental.
Leap in visual range preceded the leap to land
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