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Massive increase in visual range preceded the origin of terrestrial vertebrates.

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.

SUBMITTER: MacIver MA

PROVIDER: S-EPMC5373340 | biostudies-literature | 2017 Mar

REPOSITORIES: biostudies-literature

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Massive increase in visual range preceded the origin of terrestrial vertebrates.

MacIver Malcolm A MA Schmitz Lars L Mugan Ugurcan U Murphey Todd D TD Mobley Curtis D CD

Proceedings of the National Academy of Sciences of the United States of America 20170307 12

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 n ...[more]

PMID: 28270619

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Project description:In order to maintain visual sensitivity at all light levels, the vertebrate eye possesses a mechanism to regenerate the visual pigment chromophore 11-cis retinal in the dark enzymatically, unlike in all other taxa, which rely on photoisomerization. This mechanism is termed the visual cycle and is localized to the retinal pigment epithelium (RPE), a support layer of the neural retina. Speculation has long revolved around whether more primitive chordates, such as tunicates and cephalochordates, anticipated this feature. The two key enzymes of the visual cycle are RPE65, the visual cycle all-trans retinyl ester isomerohydrolase, and lecithin:retinol acyltransferase (LRAT), which generates RPE65's substrate. We hypothesized that the origin of the vertebrate visual cycle is directly connected to an ancestral carotenoid oxygenase acquiring a new retinyl ester isomerohydrolase function. Our phylogenetic analyses of the RPE65/BCMO and N1pC/P60 (LRAT) superfamilies show that neither RPE65 nor LRAT orthologs occur in tunicates (Ciona) or cephalochordates (Branchiostoma), but occur in Petromyzon marinus (Sea Lamprey), a jawless vertebrate. The closest homologs to RPE65 in Ciona and Branchiostoma lacked predicted functionally diverged residues found in all authentic RPE65s, but lamprey RPE65 contained all of them. We cloned RPE65 and LRATb cDNAs from lamprey RPE and demonstrated appropriate enzymatic activities. We show that Ciona ß-carotene monooxygenase a (BCMOa) (previously annotated as an RPE65) has carotenoid oxygenase cleavage activity but not RPE65 activity. We verified the presence of RPE65 in lamprey RPE by immunofluorescence microscopy, immunoblot and mass spectrometry. On the basis of these data we conclude that the crucial transition from the typical carotenoid double bond cleavage functionality (BCMO) to the isomerohydrolase functionality (RPE65), coupled with the origin of LRAT, occurred subsequent to divergence of the more primitive chordates (tunicates, etc.) in the last common ancestor of the jawless and jawed vertebrates.

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Massive increase in visual range preceded the origin of terrestrial vertebrates.

Publications

Massive increase in visual range preceded the origin of terrestrial vertebrates.

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