Eye-Transcriptome and Genome-Wide Sequencing for Scolecophidia: Implications for Inferring the Visual System of the Ancestral Snake

Author:

Gower David J1ORCID,Fleming James F23,Pisani Davide24ORCID,Vonk Freek J5,Kerkkamp Harald M I6,Peichl Leo78ORCID,Meimann Sonja7,Casewell Nicholas R9ORCID,Henkel Christiaan V610ORCID,Richardson Michael K6ORCID,Sanders Kate L11,Simões Bruno F21112ORCID

Affiliation:

1. Life Sciences, The Natural History Museum, London, United Kingdom

2. School of Life Sciences, University of Bristol, Bristol, United Kingdom

3. Institute for Advanced Biosciences, Keio University, Yamagata, Japan

4. School of Earth Sciences, University of Bristol, Bristol, United Kingdom

5. Naturalis Biodiversity Center, Leiden, The Netherlands

6. Institute of Biology, University of Leiden, Leiden, The Netherlands

7. Institute of Cellular and Molecular Anatomy, Dr. Senckenberg Anatomy, Goethe University Frankfurt, Frankfurt am Main, Germany

8. Institute of Clinical Neuroanatomy, Dr. Senckenberg Anatomy, Goethe University Frankfurt, Frankfurt am Main, Germany

9. Centre for Snakebite Research & Interventions, Liverpool School of Tropical Medicine, Liverpool, United Kingdom

10. Faculty of Veterinary Medicine, Norwegian University of Life Sciences, Ås, Norway

11. School of Biological Sciences, University of Adelaide, Adelaide, South Australia, Australia

12. School of Biological and Marine Sciences, University of Plymouth, Plymouth, United Kingdom

Abstract

Abstract Molecular genetic data have recently been incorporated in attempts to reconstruct the ecology of the ancestral snake, though this has been limited by a paucity of data for one of the two main extant snake taxa, the highly fossorial Scolecophidia. Here we present and analyze vision genes from the first eye-transcriptomic and genome-wide data for Scolecophidia, for Anilios bicolor, and A. bituberculatus, respectively. We also present immunohistochemistry data for retinal anatomy and visual opsin-gene expression in Anilios. Analyzed in the context of 19 lepidosaurian genomes and 12 eye transcriptomes, the new genome-wide and transcriptomic data provide evidence for a much more reduced visual system in Anilios than in non-scolecophidian (=alethinophidian) snakes and in lizards. In Anilios, there is no evidence of the presence of 7 of the 12 genes associated with alethinophidian photopic (cone) phototransduction. This indicates extensive gene loss and many of these candidate gene losses occur also in highly fossorial mammals with reduced vision. Although recent phylogenetic studies have found evidence for scolecophidian paraphyly, the loss in Anilios of visual genes that are present in alethinophidians implies that the ancestral snake had a better-developed visual system than is known for any extant scolecophidian.

Publisher

Oxford University Press (OUP)

Subject

Genetics,Ecology, Evolution, Behavior and Systematics

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