Diversity and Evolution of Frog Visual Opsins: Spectral Tuning and Adaptation to Distinct Light Environments.

amphibia codon-based selection models sensory biology vision research

Journal

Molecular biology and evolution
ISSN: 1537-1719
Titre abrégé: Mol Biol Evol
Pays: United States
ID NLM: 8501455

Informations de publication

Date de publication:
02 Apr 2024
Historique:
received: 12 09 2023
revised: 07 02 2024
accepted: 26 02 2024
medline: 4 4 2024
pubmed: 4 4 2024
entrez: 4 4 2024
Statut: ppublish

Résumé

Visual systems adapt to different light environments through several avenues including optical changes to the eye and neurological changes in how light signals are processed and interpreted. Spectral sensitivity can evolve via changes to visual pigments housed in the retinal photoreceptors through gene duplication and loss, differential and coexpression, and sequence evolution. Frogs provide an excellent, yet understudied, system for visual evolution research due to their diversity of ecologies (including biphasic aquatic-terrestrial life cycles) that we hypothesize imposed different selective pressures leading to adaptive evolution of the visual system, notably the opsins that encode the protein component of the visual pigments responsible for the first step in visual perception. Here, we analyze the diversity and evolution of visual opsin genes from 93 new eye transcriptomes plus published data for a combined dataset spanning 122 frog species and 34 families. We find that most species express the four visual opsins previously identified in frogs but show evidence for gene loss in two lineages. Further, we present evidence of positive selection in three opsins and shifts in selective pressures associated with differences in habitat and life history, but not activity pattern. We identify substantial novel variation in the visual opsins and, using microspectrophotometry, find highly variable spectral sensitivities, expanding known ranges for all frog visual pigments. Mutations at spectral-tuning sites only partially account for this variation, suggesting that frogs have used tuning pathways that are unique among vertebrates. These results support the hypothesis of adaptive evolution in photoreceptor physiology across the frog tree of life in response to varying environmental and ecological factors and further our growing understanding of vertebrate visual evolution.

Identifiants

pubmed: 38573520
pii: 7639264
doi: 10.1093/molbev/msae049
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© The Author(s) 2024. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.

Auteurs

Ryan K Schott (RK)

Department of Biology and Centre for Vision Research, York University, Toronto, Ontario, Canada.
Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC, USA.

Matthew K Fujita (MK)

Department of Biology, Amphibian and Reptile Diversity Research Center, The University of Texas at Arlington, Arlington, TX, USA.

Jeffrey W Streicher (JW)

Natural History Museum, London, UK.

David J Gower (DJ)

Natural History Museum, London, UK.

Kate N Thomas (KN)

Department of Biology, Amphibian and Reptile Diversity Research Center, The University of Texas at Arlington, Arlington, TX, USA.
Natural History Museum, London, UK.

Ellis R Loew (ER)

Department of Biomedical Sciences, Cornell University College of Veterinary Medicine, Ithaca, NY, USA.

Abraham G Bamba Kaya (AG)

Institute de Recherches Agronomiques et Forestières, Libreville, Gabon.

Gabriela B Bittencourt-Silva (GB)

Natural History Museum, London, UK.

C Guillherme Becker (C)

Department of Biology and One Health Microbiome Center, Center for Infectious Disease Dynamics, The Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, USA.

Diego Cisneros-Heredia (D)

Laboratorio de Zoología Terrestre, Instituto de Biodiversidad Tropical IBIOTROP, Colegio de Ciencias Biológicas y Ambientales, Universidad San Francisco de Quito USFQ, Quito, Ecuador.

Simon Clulow (S)

Centre for Conservation Ecology and Genomics, Institute for Applied Ecology, University of Canberra, Bruce, ACT, Australia.

Mateo Davila (M)

Laboratorio de Zoología Terrestre, Instituto de Biodiversidad Tropical IBIOTROP, Colegio de Ciencias Biológicas y Ambientales, Universidad San Francisco de Quito USFQ, Quito, Ecuador.

Thomas J Firneno (TJ)

Department of Biological Sciences, University of Denver, Denver, USA.

Célio F B Haddad (CFB)

Department of Biodiversity and Center of Aquaculture-CAUNESP, I.B., São Paulo State University, Rio Claro, São Paulo, Brazil.

Sunita Janssenswillen (S)

Amphibian Evolution Lab, Biology Department, Vrije Universiteit Brussel, Brussels, Belgium.

Jim Labisko (J)

Natural History Museum, London, UK.
Centre for Biodiversity and Environment Research, Department of Genetics, Evolution and Environment, University College London, London, UK.
Island Biodiversity and Conservation Centre, University of Seychelles, Mahé, Seychelles.

Simon T Maddock (ST)

Natural History Museum, London, UK.
Island Biodiversity and Conservation Centre, University of Seychelles, Mahé, Seychelles.
School of Natural and Environmental Sciences, Newcastle University, Newcastle Upon Tyne, UK.

Michael Mahony (M)

Department of Biological Sciences, The University of Newcastle, Newcastle 2308, Australia.

Renato A Martins (RA)

Programa de Pós-graduação em Conservação da Fauna, Universidade Federal de São Carlos, São Carlos, Brazil.

Christopher J Michaels (CJ)

Independent Scholar, London, UK.

Nicola J Mitchell (NJ)

School of Biological Sciences, The University of Western Australia, Crawley, WA 6009, Australia.

Daniel M Portik (DM)

Department of Herpetology, California Academy of Sciences, San Francisco, CA, USA.

Ivan Prates (I)

Department of Biology, Lund University, Lund, Sweden.

Kim Roelants (K)

Amphibian Evolution Lab, Biology Department, Vrije Universiteit Brussel, Brussels, Belgium.

Corey Roelke (C)

Department of Biology, Amphibian and Reptile Diversity Research Center, The University of Texas at Arlington, Arlington, TX, USA.

Elie Tobi (E)

Gabon Biodiversity Program, Center for Conservation and Sustainability, Smithsonian National Zoo and Conservation Biology Institute, Gamba, Gabon.

Maya Woolfolk (M)

Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC, USA.
Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA, USA.

Rayna C Bell (RC)

Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC, USA.
Department of Herpetology, California Academy of Sciences, San Francisco, CA, USA.

Classifications MeSH