Evolutionary loss of cone photoreception in balaenid whales reveals circuit stability in the mammalian retina
ABSTRACT The classical understanding of mammalian vision is that it occurs through “duplex” retinae containing both rod and cone photoreceptors, the signals from which are processed through rod‐ and/or cone‐specific signaling pathways. The recent discovery of rod monochromacy in some cetacean lineag...
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crwiley:10.1002/cne.23996 2024-06-02T08:03:53+00:00 Evolutionary loss of cone photoreception in balaenid whales reveals circuit stability in the mammalian retina Schweikert, Lorian E. Fasick, Jeffry I. Grace, Michael S. Consortium for Wildlife Bycatch Reduction, New England Aquarium, under the National Oceanic and Atmospheric Administration National Science Foundation Graduate Research Fellowship 2016 http://dx.doi.org/10.1002/cne.23996 https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1002%2Fcne.23996 https://onlinelibrary.wiley.com/doi/pdf/10.1002/cne.23996 https://onlinelibrary.wiley.com/doi/full-xml/10.1002/cne.23996 https://onlinelibrary.wiley.com/doi/am-pdf/10.1002/cne.23996 en eng Wiley http://onlinelibrary.wiley.com/termsAndConditions#am http://onlinelibrary.wiley.com/termsAndConditions#vor Journal of Comparative Neurology volume 524, issue 14, page 2873-2885 ISSN 0021-9967 1096-9861 journal-article 2016 crwiley https://doi.org/10.1002/cne.23996 2024-05-03T10:44:28Z ABSTRACT The classical understanding of mammalian vision is that it occurs through “duplex” retinae containing both rod and cone photoreceptors, the signals from which are processed through rod‐ and/or cone‐specific signaling pathways. The recent discovery of rod monochromacy in some cetacean lineages provides a novel opportunity to investigate the effects of an evolutionary loss of cone photoreception on retinal organization. Sequence analysis of right whale ( Eubalaena glacialis; family Balaenidae) cDNA derived from long‐wavelength sensitive (LWS) cone opsin mRNA identified several mutations in the opsin coding sequence, suggesting the loss of cone cell function, but maintenance of non‐photosensitive, cone opsin mRNA‐expressing cells in the retina. Subsequently, we investigated the retina of the closely related bowhead whale ( Balaena mysticetus; family Balaenidae) to determine how the loss of cone‐mediated photoreception affects light signaling pathways in the retina. Anti‐opsin immunofluorescence demonstrated the total loss of cone opsin expression in B. mysticetus , whereas light microscopy, transmission electron microscopy, and bipolar cell (protein kinase C‐α [PKC‐α] and recoverin) immunofluorescence revealed the maintenance of cone soma, putative cone pedicles, and both rod and cone bipolar cell types. These findings represent the first immunological and anatomical evidence of a naturally occurring rod‐monochromatic mammalian retina, and suggest that despite the loss of cone‐mediated photoreception, the associated cone signaling structures (i.e., cone synapses and cone bipolar cells) may be maintained for multichannel rod‐based signaling in balaenid whales. J. Comp. Neurol. 524:2873–2885, 2016. © 2016 Wiley Periodicals, Inc. Article in Journal/Newspaper Balaena mysticetus bowhead whale Eubalaena glacialis Wiley Online Library Journal of Comparative Neurology 524 14 2873 2885 |
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Wiley Online Library |
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crwiley |
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English |
description |
ABSTRACT The classical understanding of mammalian vision is that it occurs through “duplex” retinae containing both rod and cone photoreceptors, the signals from which are processed through rod‐ and/or cone‐specific signaling pathways. The recent discovery of rod monochromacy in some cetacean lineages provides a novel opportunity to investigate the effects of an evolutionary loss of cone photoreception on retinal organization. Sequence analysis of right whale ( Eubalaena glacialis; family Balaenidae) cDNA derived from long‐wavelength sensitive (LWS) cone opsin mRNA identified several mutations in the opsin coding sequence, suggesting the loss of cone cell function, but maintenance of non‐photosensitive, cone opsin mRNA‐expressing cells in the retina. Subsequently, we investigated the retina of the closely related bowhead whale ( Balaena mysticetus; family Balaenidae) to determine how the loss of cone‐mediated photoreception affects light signaling pathways in the retina. Anti‐opsin immunofluorescence demonstrated the total loss of cone opsin expression in B. mysticetus , whereas light microscopy, transmission electron microscopy, and bipolar cell (protein kinase C‐α [PKC‐α] and recoverin) immunofluorescence revealed the maintenance of cone soma, putative cone pedicles, and both rod and cone bipolar cell types. These findings represent the first immunological and anatomical evidence of a naturally occurring rod‐monochromatic mammalian retina, and suggest that despite the loss of cone‐mediated photoreception, the associated cone signaling structures (i.e., cone synapses and cone bipolar cells) may be maintained for multichannel rod‐based signaling in balaenid whales. J. Comp. Neurol. 524:2873–2885, 2016. © 2016 Wiley Periodicals, Inc. |
author2 |
Consortium for Wildlife Bycatch Reduction, New England Aquarium, under the National Oceanic and Atmospheric Administration National Science Foundation Graduate Research Fellowship |
format |
Article in Journal/Newspaper |
author |
Schweikert, Lorian E. Fasick, Jeffry I. Grace, Michael S. |
spellingShingle |
Schweikert, Lorian E. Fasick, Jeffry I. Grace, Michael S. Evolutionary loss of cone photoreception in balaenid whales reveals circuit stability in the mammalian retina |
author_facet |
Schweikert, Lorian E. Fasick, Jeffry I. Grace, Michael S. |
author_sort |
Schweikert, Lorian E. |
title |
Evolutionary loss of cone photoreception in balaenid whales reveals circuit stability in the mammalian retina |
title_short |
Evolutionary loss of cone photoreception in balaenid whales reveals circuit stability in the mammalian retina |
title_full |
Evolutionary loss of cone photoreception in balaenid whales reveals circuit stability in the mammalian retina |
title_fullStr |
Evolutionary loss of cone photoreception in balaenid whales reveals circuit stability in the mammalian retina |
title_full_unstemmed |
Evolutionary loss of cone photoreception in balaenid whales reveals circuit stability in the mammalian retina |
title_sort |
evolutionary loss of cone photoreception in balaenid whales reveals circuit stability in the mammalian retina |
publisher |
Wiley |
publishDate |
2016 |
url |
http://dx.doi.org/10.1002/cne.23996 https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1002%2Fcne.23996 https://onlinelibrary.wiley.com/doi/pdf/10.1002/cne.23996 https://onlinelibrary.wiley.com/doi/full-xml/10.1002/cne.23996 https://onlinelibrary.wiley.com/doi/am-pdf/10.1002/cne.23996 |
genre |
Balaena mysticetus bowhead whale Eubalaena glacialis |
genre_facet |
Balaena mysticetus bowhead whale Eubalaena glacialis |
op_source |
Journal of Comparative Neurology volume 524, issue 14, page 2873-2885 ISSN 0021-9967 1096-9861 |
op_rights |
http://onlinelibrary.wiley.com/termsAndConditions#am http://onlinelibrary.wiley.com/termsAndConditions#vor |
op_doi |
https://doi.org/10.1002/cne.23996 |
container_title |
Journal of Comparative Neurology |
container_volume |
524 |
container_issue |
14 |
container_start_page |
2873 |
op_container_end_page |
2885 |
_version_ |
1800748481373011968 |