Ontogeny of Ultraviolet-Sensitive Cones
in the Retina of Rainbow Trout
(Oncorhynchus mykiss)
W. TED ALLISON,
1
STEPHEN G. DANN,
1
JON VIDAR HELVIK,
2
CLARRISA BRADLEY,
1
HEATHER D. MOYER,
1
AND CRAIG W. HAWRYSHYN
1
*
1
Department of Biology, University of Victoria, Victoria,
British Columbia V8W 3N5, Canada
2
Department of Molecular Biology, University of Bergen, 5020 Bergen, Norway
ABSTRACT
In order to facilitate emerging models of retinal development, we developed electroreti-
nogram and in situ hybridization protocols to examine the ontogeny of photoreceptors in the
retina of a land-locked salmonid, the rainbow trout (Oncorhynchus mykiss). We cloned cDNA
fragments corresponding to the rod opsin and each of the four cone opsin gene families, which
we utilized to produce riboprobes. We established the specificity of the in situ hybridization
protocol by examining subcellular signal localization and through double-labeling experi-
ments. We confirm the assumption that the accessory corner cones in the square mosaic are
the ultraviolet wavelength-sensitive (UVS) cone photoreceptor (i.e., they express an SWS1
opsin) and observed UVS cones throughout the retina of small trout. Larger fish have a
decrease in sensitivity to short wavelength light stimuli and the distribution of UVS cones in
the mature retina is limited to the dorsal-temporal quadrant. These larger fish also possess
differentiated UVS cones in the peripheral germinal zone (PGZ), including within areas
peripheral to mature retina lacking UVS cones. These data are consistent with the loss of
putative UVS cones from the PGZ of a migratory salmonid of another genus, and thus the
disappearance of UVS cones appears to be general to the Family Salmonidae, regardless of
life history strategy. The generation, differentiation, and subsequent loss of UVS cones in the
smolt PGZ is a dramatic example of the supposition that the mechanisms of PGZ development
recapitulate the retinal embryogenesis of that species. J. Comp. Neurol. 461:294 –306, 2003.
© 2003 Wiley-Liss, Inc.
Indexing terms: teleost; in situ hybridization; proliferative growth zone; retinal development;
electroretinogram
The vertebrate retina is a part of the central ner-
vous system (CNS) that has served as an effective ex-
ample of CNS function, development, and evolution.
The teleost retina has various properties, including a
layered structure, a regular mosaic of photoreceptors,
and continuous growth throughout life (Lyall, 1957a,b),
which have been particularly valuable in this regard.
For example, the study of the visual system in goldfish
and carp has revealed much about the mechanisms
underlying color vision (Kamermans and Spekreijse,
1999), whereas the zebrafish retina has become a pop-
ular model to study CNS development (Bilotta and
Saszik, 2001; Li, 2001). Furthermore, the diversity of
habitats and life histories that teleosts have exploited
allow an examination of the evolution of CNS function
and development.
Salmonids, including salmon and trout, comprise a
large group of closely related species with a variety of
Grant sponsor: Alzheimer Society of Canada; Grant sponsor: Canadian
Institute of Health Research; Institute of Aging Fellowship (W.E.A.); Grant
sponsor: Natural Sciences and Engineering Research Council of Canada
(NSERC) Postgraduate Fellowship (S.G.D.); Grant sponsor: NSERC Un-
dergraduate Research Award (C.B., H.D.M.); Grant sponsor: NSERC Op-
erating and Equipment Grant (C.W.H.).
*Correspondence to: Craig W. Hawryshyn, Department of Biology, Uni-
versity of Victoria, Victoria, British Columbia V8W 3N5, Canada.
E-mail:chawrysh@uvic.ca
Received 4 August 2002; Revised 12 December 2002; Accepted 5 January
2003
DOI 10.1002/cne.10682
Published online the week of May 12, 2003 in Wiley InterScience (www.
interscience.wiley.com).
THE JOURNAL OF COMPARATIVE NEUROLOGY 461:294 –306 (2003)
© 2003 WILEY-LISS, INC.