Adaptive Gene Loss Reflects Differences in the Visual Ecology of Basal Vertebrates

Davies, Wayne L., Collin, Shaun P. and Hunt, David M. (2009) Adaptive Gene Loss Reflects Differences in the Visual Ecology of Basal Vertebrates. Molecular Biology and Evolution, 26 8: 1803-1809. doi:10.1093/molbev/msp089


Author Davies, Wayne L.
Collin, Shaun P.
Hunt, David M.
Title Adaptive Gene Loss Reflects Differences in the Visual Ecology of Basal Vertebrates
Journal name Molecular Biology and Evolution   Check publisher's open access policy
ISSN 0737-4038
Publication date 2009-08-01
Year available 2009
Sub-type Article (original research)
DOI 10.1093/molbev/msp089
Open Access Status Not yet assessed
Volume 26
Issue 8
Start page 1803
End page 1809
Total pages 7
Editor Marcy Uyenoyama
Place of publication Oxford, England
Publisher Oxford University Press
Language eng
Subject C1
110906 Sensory Systems
060805 Animal Neurobiology
060409 Molecular Evolution
830102 Aquaculture Fin Fish (excl. Tuna)
Abstract The agnathans (lampreys and hagfishes) are representatives of the jawless fishes and constitute the first lineage of extant vertebrates to evolve within chordate phylogenetic history. Previously, we showed that the southern hemisphere pouched lamprey Geotria australis has the potential for pentachromacy with the expression of five visual pigment (opsin) genes (LWS, SWS1, SWS2, RhA, and RhB) in five different cone-like photoreceptors for life in a brightly lit environment exposed to a broad spectrum of light. In contrast, the northern hemisphere sea lamprey Petromyzon marinus dwells in a wide range of depths that are relatively deeper than the epipelagic waters inhabited by G. australis. Thus, the light levels of the habitat in which the sea lamprey resides are greatly diminished and different regions of the light spectrum are differentially absorbed. Therefore, the visual systems of these two species of lamprey constitute a natural experiment in which to study the selection pressures underlying opsin gene expression and the evolution of color discrimination. By analyzing the opsin genes of P. marinus, we show the expression of two intact retinal opsins, RhA and LWS, which, when regenerated with 11-cis retinal, give peak spectral sensitivities (lambda(max) values) of 501 and 536 nm, respectively. In contrast to G. australis, the genome of P. marinus possesses remnants of SWS1 and SWS2 pseudogenes, which with the loss of RhB, suggests that P. marinus is a dichromat. Using site-directed mutagenesis, we show that a single amino acid substitution (Ser to Pro) at site 164 is responsible for a blue shift of 19 nm of the LWS visual pigment of P. marinus compared with G. australis, which may reflect habitat differences between the two species. Based on these studies, we propose that gene loss (or duplication) and subsequent mutation plays an important role in the evolution of color vision and that the complement and tuning of these visual pigments reflect the ecology and light environment of these phylogenetically basal vertebrates.
Formatted abstract
The agnathans (lampreys and hagfishes) are representatives of the jawless fishes and constitute the first lineage of extant vertebrates to evolve within chordate phylogenetic history. Previously, we showed that the southern hemisphere pouched lamprey Geotria australis has the potential for pentachromacy with the expression of five visual pigment (opsin) genes (LWS, SWS1, SWS2, RhA, and RhB) in five different cone-like photoreceptors for life in a brightly lit environment exposed
to a broad spectrum of light. In contrast, the northern hemisphere sea lamprey Petromyzon marinus dwells in a wide range of depths that are relatively deeper than the epipelagic waters inhabited by G. australis. Thus, the light levels of the habitat in which the sea lamprey resides are greatly diminished and different regions of the light spectrum are differentially absorbed. Therefore, the visual systems of these two species of lamprey constitute a natural experiment in which to study the selection pressures underlying opsin gene expression and the evolution of color discrimination. By analyzing the opsin genes of P. marinus, we show the expression of two intact retinal opsins, RhA and LWS, which, when regenerated with 11-cis retinal, give peak spectral sensitivities (kmax values) of 501 and 536 nm, respectively. In contrast to G. australis, the genome of P. marinus possesses remnants of SWS1 and SWS2 pseudogenes, which with the loss of RhB, suggests that P. marinus is a dichromat. Using site-directed mutagenesis, we show that a single amino acid substitution (Ser to Pro) at site 164 is responsible for a blue shift of 19 nm of the LWS visual pigment of P. marinus compared with G. australis, which may reflect habitat differences between the two species. Based on these studies, we propose that gene loss (or duplication) and subsequent mutation plays an important role in the evolution of color vision and that the complement and tuning of these visual pigments reflect the ecology and light environment of these phylogenetically basal vertebrates.
Keyword Evolution
Lamprey
Life Cycle
Visual Pigment
Opsin
Q-Index Code C1
Q-Index Status Confirmed Code

Document type: Journal Article
Sub-type: Article (original research)
Collections: 2010 Higher Education Research Data Collection
School of Biomedical Sciences Publications
 
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Created: Fri, 28 Aug 2009, 20:00:38 EST by Shirley Rey on behalf of School of Biomedical Sciences