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Nießner 2016 cryptochrome 1 in blue cones of mammals supplement

Authors:
  • Max Planck Institute for Neurobiology of Behavior
  • Health and Medical University Potsdam
1
Supplementary Information
Cryptochrome 1 in Retinal Cone Photoreceptors Suggests
a Novel Functional Role in Mammals
Christine Nießner, Susanne Denzau, Erich Pascal Malkemper, Julia Christina Gross, Hynek
Burda, Michael Winklhofer, Leo Peichl
Table S1. Retinal cryptochrome 1 and S1 opsin labeling in the species studied. The two left columns show
representative high-resolution micrographs of the layer of photoreceptor outer segments in vertical retinal
sections that had been double immunofluorescence-labeled for Cry1* (green) and S1 opsin (magenta). Each
image pair shows exactly the same field, photographed with the respective fluorescence filters. Where Cry1* is
labeled, it is located in the opsin-containing outer segments of the S1 cones. The right column gives the species
names and tissue sources. Species are grouped taxonomically. Reference numbers refer to Supplementary
References.
Cry1*
S1 opsin
Species
Metatheria
Didelphimorphia
Gray short-tailed opossum, Monodelphis domestica
Adult, post mortem experimental material from breeding colony.
Courtesy L. Krubitzer & J. Luu, University of California Davis, CA, USA
Eutheria
Afrosoricida
Lesser hedgehog tenrec, Echinops telfairi
Adult, post mortem experimental material from breeding colony.
Courtesy H. Künzle, Ludwig Maximilians University, Munich, Germany
Tubulidentata
Aardvark, Orycteropus afer
Collection material. Courtesy P. Němec, Dept. of Zoology, Charles University,
Prague, CZ
Hyracoidea
Rock hyrax, Procavia capensis
Collection material. Courtesy K. Moutairou, National University of Benin,
Cotonou, Benin
2
Proboscidea
Asian elephant, Elephas maximus
Adult, autopsy material. Courtesy G. Wibbelt, Leibniz Institute for Zoo and
Wildlife Research, Berlin, Germany
African bush elephant, Loxodonta africana
Adult, autopsy material. Courtesy G. Wibbelt, Leibniz Institute for Zoo and
Wildlife Research, Berlin, Germany
Pilosa
Southern tamandua, Tamandua tetradactyla (has no S1 cones; own
observation)
Autopsy material. Courtesy G. Wibbelt, Leibniz Institute for Zoo and Wildlife
Research, Berlin, Germany
Scandentia
Tree shrew, Tupaia belangeri
Adult, post mortem experimental material from a breeding colony
at MPI for Brain Research
Dermoptera
Colugo (flying lemur), Galeopterus variegatus
Wild adult found dead. Courtesy N. Lim, National University of Singapore &
Raffles Museum of Biodiversity Research, Singapore
Primates
Gray mouse lemur, Microcebus murinus
Adult, post mortem experimental material. Courtesy A. Kaiser, Veterinary
University Hannover, Germany
White sifaka, Propithecus verreauxi
Autopsy material. Courtesy P. Kappeler, German Primate Center Göttingen,
Germany
Red-fronted lemur, Eulemur rufifrons
Autopsy material. Courtesy P. Kappeler, German Primate Center Göttingen,
Germany
Common marmoset, Callithrix jacchus
Adult, post mortem experimental material. Courtesy C. Puller, MPI for Brain
Research
Owl monkey, Aotus sp. (has no S1 cones1)
Adult female, post mortem experimental material. Courtesy A. Hendrickson,
University of Washington, Seattle, WA, USA
3
King colobus, Colobus polykomos
Adult, post mortem experimental material. Courtesy K. Mätz-Rensing, German
Primate Center Göttingen, Germany
Nilgiri langur, Trachypithecus johnii
Adult, post mortem experimental material. Courtesy K. Mätz-Rensing, German
Primate Center Göttingen, Germany
Green monkey, Chlorocebus sabaeus
Adult, post mortem experimental material. Courtesy R. Plesker, Paul-Ehrlich-
Institut Langen, Germany
Rhesus macaque, Macaca mulatta
Adult, post mortem experimental material. Courtesy German Primate Center
Göttingen, Germany
Crab-eating macaque, Macaca fascicularis
Old female, post mortem experimental material. Courtesy M. Munk, MPI for
Brain Research
Bornean orangutan, Pongo pygmaeus
Old male, autopsy material. Courtesy Zoo Frankfurt/M., Morphisto GmbH and
Senckenberg Museum Frankfurt/M., Germany
Spectral tarsier, Tarsius tarsier
Adult, post mortem experimental material. Courtesy A. Hendrickson, University
of Washington, Seattle, WA, USA
Rodentia
Red squirrel, Sciurus vulgaris
Eye collection of the MPI for Brain Research
Grey squirrel, Sciurus carolinensis
Adult, culled animal. Courtesy UK Forestry Commission & G. Jeffery,
University College London, UK
Eastern (Bryant's) fox squirrel, Sciurus niger
Post mortem experimental material. Courtesy N. Tararova, Medical School,
Cleveland University, OH, USA
Woodchuck, Marmota monax
Post mortem experimental material. Courtesy P. Dammann, Central
Animal Laboratory, Essen University Medical School, Germany
Fat dormouse, Glis glis (has no S1 cones2)
Eye collection of the MPI for Brain Research
4
Laboratory mouse, Mus musculus
Adult, strain C57BL/6, breeding colony at MPI for Brain Research
Laboratory rat, Rattus norvegicus
Adult, breeding colony at MPI for Brain Research
Wood mouse, Apodemus sylvaticus
Adult, killed for unrelated study at Dept. of General Zoology, University
Duisburg-Essen, Germany
Common vole, Microtus arvalis
Courtesy S.A. Romanenko & A. Graphodaskii, Institute of Molecular and
Cellular Biology, SB RAS, Novosibirsk, Russia
European water vole, Arvicola terrestris
Courtesy S.A. Romanenko & A. Graphodaskii, Institute of Molecular and
Cellular Biology, SB RAS, Novosibirsk, Russia
Bank vole, Myodes (Clethrionomys) glareolus
Courtesy S.A. Romanenko & A. Graphodaskii, Institute of Molecular and
Cellular Biology, SB RAS, Novosibirsk, Russia
Grey red-backed vole, Myodes (Clethrionomys) rufocanus
Courtesy S.A. Romanenko & A. Graphodaskii, Institute of Molecular and
Cellular Biology, SB RAS, Novosibirsk, Russia
Deer mouse, Peromyscus maniculatus
Adult, breeding colony at MPI for Brain Research
Domestic guinea pig, Cavia porcellus
Adult, from animal house at MPI for Brain Research
Naked mole rat, Heterocephalus glaber (subterranean)
Adult, killed for unrelated study at Dept. of General Zoology, University
Duisburg-Essen, Germany
Ansell's mole rat, Fukomys anselli (subterranean)
Adult, killed for unrelated study at Dept. of General Zoology, University
Duisburg-Essen, Germany
Mechow's mole rat, Fukomys mechowii (subterranean)
Adult, killed for unrelated study at Dept. of General Zoology, University
Duisburg-Essen, Germany
Chinchilla, Chinchilla lanigera
Adult, eye collection of the MPI for Brain Research
5
Lagomorpha
Domestic rabbit, Oryctolagus cuniculus
Adult, from animal house at MPI for Brain Research
Eulipotyphla
Southern white-breasted hedgehog, Erinaceus concolor
Courtesy S.A. Romanenko & A. Graphodaskii, Institute of Molecular and
Cellular Biology, SB RAS, Novosibirsk, Russia
Common shrew, Sorex araneus
Courtesy S.A. Romanenko & A. Graphodaskii, Institute of Molecular and
Cellular Biology, SB RAS, Novosibirsk, Russia
Chiroptera
Seba's short-tailed bat, Carollia perspicillata
Post mortem experimental material. Courtesy B. Müller, MPI for
Brain Research & M. Kössl, University Frankfurt/M., Germany
Pallas' long-tongued bat, Glossophaga soricina
Post mortem experimental material. Courtesy B. Müller, MPI for
Brain Research
Peters's wrinkle-lipped bat, Mormopterus jugularis
Collection material. Courtesy S.M. Goodman, Field Museum of Natural History,
Chicago, IL, USA, & WWF, Antananarivo, Madagascar
Velvety free-tailed bat, Mollossus mollossus
Post mortem experimental material. Courtesy B. Müller, MPI for Brain Research
& M. Kössl, University Frankfurt/M., Germany
Madagascar rousette, Rousettus madagascariensis (has no S1 cones3)
Collection material. Courtesy S.M. Goodman, Field Museum of Natural History,
Chicago, IL, USA, & WWF, Madagascar
Mauritian flying fox, Pteropus niger
Collection material. Courtesy S.M. Goodman, Field Museum of Natural History,
Chicago, IL, USA, & WWF, Madagascar
Madagascan flying fox, Pteropus rufus
Collection material. Courtesy S.M. Goodman, Field Museum of Natural History,
Chicago, IL, USA, & WWF, Madagascar
Carnivora
Domestic dog, Canis lupus familiaris
Adult Beagle-Setter-Mix, post mortem experimental material. Courtesy K.
Stieger, Giessen University Eye Clinic, Giessen, Germany
6
Grey wolf, Canis lupus
Adult, euthanized animal. Courtesy K. Burow, Wildlife Park ’Alte Fasanerie’,
Hanau, Germany
Raccoon dog, Nyctereutes procyonoides
Adult. Eye collection of the MPI for Brain Research
Red fox, Vulpes vulpes
Adult, hunted animal. Courtesy E. Noll, MPI for Brain Research
Arctic fox, Vulpes (Alopex) lagopus
Young adult. Eye collection of the MPI for Brain Research
European otter, Lutra lutra
Adult, roadkill. Courtesy H. Ansorge, Staatliches Museum für Naturkunde,
Görlitz, Germany
Sea otter, Enhydra lutris lutris
Adult, autopsy material from stranded animal. Courtesy P. Tuomi, Alaska Sea
Life Center, Seward, AK, USA
Ferret, Mustela putorius furo
Young animal, post mortem experimental material. Courtesy M.
Leinweber, MPI for Neurobiology, Munich, Germany
European badger, Meles meles
Adult, roadkill. Courtesy E. Noll, MPI for Brain Research
Beech marten, Martes foina
Adult, roadkill. Courtesy E. Noll, MPI for Brain Research
Brown bear, Ursus arctos
Adult hunted animal. Courtesy A. Friebe, Scandinavian Brown Bear Research
Project, Kvarnberg, Sweden
Polar bear, Ursus (Thalarctos) maritimus
Adult, killed for an unrelated project. Courtesy K.M. Kovacs, Norwegian Polar
Institute, Tromsø, Norway
Coati, Nasua nasua
Adult, post mortem experimental material. Courtesy B. Pohl, Veterinary
University Hannover, Germany
Crab-eating raccoon, Procyon cancrivorous (has no S1 cones4,5)
Adult, post mortem experimental material. Courtesy B. Pohl,
Veterinary University Hannover, Germany
7
Australian Fur Seal, Arctocephalus pusillus (has no S1 cones6)
Adult, autopsy material. Courtesy Taronga Zoo Sydney & U. Grünert, University
of Sydney, Australia
Harbour seal, Phoca vitulina (has no S1 cones7,8)
2-week pup, autopsy material. Courtesy Seal Centre Friedrichskoog, Germany
Yellow mongoose, Cynictis penicillata
Post mortem experimental material. Courtesy M. Manser, Inst. of Evolutionary
Biology & Environmental Studies, University of Zurich, Switzerland
Grandidier's mongoose, Galidictis grandidieri
Collection material. Courtesy S.M. Goodman, Field Museum of Natural History,
Chicago, IL, USA, & WWF, Madagascar
Domestic cat, Felis catus
Adult, post mortem experimental material, MPI for Brain Research
Leopard, Panthera pardus
Adult, autopsy material. Courtesy Veterinary Pathology Institute of Leipzig
University, Leipzig, Germany
Lion, Panthera leo leo
Adult, autopsy material. Courtesy Veterinary Pathology Institute of Leipzig
University, Leipzig, Germany
Siberian tiger, Panthera tigris altaica
Adult, autopsy material. Courtesy Veterinary Pathology Institute of Leipzig
University, Leipzig, Germany
Perissodactyla
Domestic donkey, Equus asinus asinus
Adult, slaughterhouse material. Courtesy J. González-Soriano, Universidad
Complutense, Madrid, Spain
Domestic horse, Equus caballus
Old animal, slaughterhouse material
Grevy's zebra, Equus grevyi
Culled animal. Courtesy J. Bhattacharjee, Egerton University, Njoro,
Kenya
Tapir, Tapirus terrestris
Adult, autopsy material. Courtesy G. Wibbelt, Leibniz Institute for Zoo and
Wildlife Research, Berlin, Germany
8
Black rhinoceros, Diceros bicornis
Juvenile, autopsy material. Courtesy Veterinary Pathology Institute of Leipzig
University, Leipzig, Germany
Artiodactyla
Dama gazelle, Nanger dama
Adult, autopsy material. Courtesy Veterinary Pathology Institute of Leipzig
University, Leipzig, Germany
Domestic goat, Capra aegagrus hircus
Slaughterhouse material
Mouflon, Ovis orientalis
Culled animal. Courtesy E. Noll, MPI for Brain Research
Domestic cattle, Bos taurus
Slaughterhouse material
Roe deer, Capreolus capreolus
Adult, hunted animal. Courtesy E. Noll, MPI for Brain Research
Red deer, Cervus elaphus
Adult, hunted animal. Courtesy E. Noll, MPI for Brain Research
Sika deer, Cervus nippon
Juvenile, culled animal. Courtesy K. Burow, Wildlife Park `Alte Fasanerie',
Hanau, Germany
Fallow deer, Dama dama
Juvenile, hunted animal. Courtesy E. Noll, MPI for Brain Research
Llama, Lama Glama
Juvenile, autopsy material. Courtesy I. Gunsser, Ludwig Maximilians University,
Munich, Germany
Dromedary camel, Camelus dromedarius
Adult, autopsy material. Courtesy G. Wibbelt, Leibniz Institute for Zoo and
Wildlife Research, Berlin, Germany
Pygmy hippopotamus, Choeropsis liberiensis
Adult, autopsy material. Courtesy G. Wibbelt, Leibniz Institute for Zoo and
Wildlife Research, Berlin, Germany
9
Wild boar, Sus scrofa
Adult, hunted animal. Courtesy E. Noll, MPI for Brain Research
Cetacea
Long-finned pilot whale, Globicephala melas (has no S1 cones6,9)
Courtesy G. Behrmann, Alfred Wegener Institute for Polar and Marine Research,
Bremerhaven, Germany
Common minke whale, Balaenoptera acutorostrata (has no cone opsins9,10)
Animal killed for an unrelated project. Courtesy K.M. Kovacs, Norwegian Polar
Institute, Tromsø, Norway
Table S2. Amino acid sequence of the antigen of the bird Cry1a antiserum compared with the sequences
of Cry1 in different mammalian species. Identical amino acids are given in red.
Cry1
labeling in
retinal
sections
Part of sequence
GenBank
RPNPEEETQSVGPKVQRQST
-
RPRQEEETQSINPKVQRQST*
XP_003342014.1
-
RPSQDEETQTLGPKVQRQST*
XP_003405361.1
+
RPSQEEDTQSIGPKVQRQST
NP_001181088.1
-
RPSQEEDTQSIGPKVQRQST
BAB72089.1
-
RPSQEEDAQSVGPKVQRQS
NP_031797.1
-
RPSQEEDAQSVGPKVQRQS
EDM17107.1
-
RPSQEEDAQSTGHKIQRQS*
XP_003462370.1
-
RPSQEEDAQSIGPKLQRQST
EHB16315.1
-
RPSQEEDTQSIGPKVQRQST*
XP_002711467.1
+
RPSEEEDTQTISPKVQRQST*
XP_862753.1
+
RPSEEEDTQSIGSKVQRQST
XP_862753.1
-
RPSQEEDTQSIGPKVQRQS*
XP_003989258.1
-
RPGPEEDTQGIGPKVQRQST*
XP_001499263.1
-
RPSQEEDTQSIGPKVQRQST
NP_001098885.1
-
RPSQEEDTQSIIGPKVQRQST*
XP_003126127.1
* predicted
10
Figure S1. Phylogenetic tree for the Carnivora species studied. Simplified phylogenetic tree of the order
Carnivora showing the relationships between the species tested in this study; other carnivore taxa are not
included. The horizontal positions of the branch points roughly reflect the divergence times of the respective
taxa. Tree data are taken from11, where more accurate presentations of the divergence times are given. Filled
coloured circles indicate the presence of S1 opsin and Cry1*, respectively, open circles indicate their absence
(c.f. Supplementary Table S1).
11
Figure S2. Examples of the retinae of different species labeled for Cry1 and S1 opsin. Vertical retinal
sections of selected mammals with differing S1 opsin and Cry1* expression patterns. Each pair of images shows
the same frame, exposed for Cry1* immunofluorescence (rendered in green) and S1 opsin immunofluorescence
(rendered in magenta). Cry1* label is only present in the retina of red fox, European otter and polar bear, and it
is restricted to the outer segments of the S1 cones. S1 opsin label is present in all illustrated species except the
long-finned pilot whale, which has no S1 opsin. The retinal layers indicated exemplarily in two panels are:
OS/IS, photoreceptor outer and inner segments; ONL, outer nuclear layer; OPL, outer plexiform layer; INL,
inner nuclear layer; IPL, inner plexiform layer; GCL, ganglion cell layer. The scale bar represents 50 µm and
applies to all panels.
12
Figure S3. Examples of the retinae of primates labeled for Cry1 and S1 opsin. Retinal flatmounts double-
labeled for Cry1* (left column) and S1 opsin (middle column) or L opsin (bottom row), the corresponding
merges are shown in the right column. Cry1* label associated with S1 cones differs between the species. In the
red-fronted lemur, Cry1* label is weak (some marked by arrows), in the green monkey no Cry1* signal is
visible. In the macaques there is strong Cry1* label in the S cones, but the crab-eating macaque shows additional
Cry1* label in rare structures (arrows) that are neither S1 cones nor L cones; for details see text. The scale bar
represents 50 µm and applies to all panels.
13
Figure S4. Western Blots of cell fractionated retinae of dog and mouse. The fractions are indicated on top,
the fraction markers on the left. Cry1 is found in the cytosolic and the membrane fraction in dogs, and in the
membrane and the nuclear fraction in mice. Because of increasing dissolving strength of fractionation buffers,
some markers are carried over into subsequent fractions, e.g. E-cadherin or H3. Actin is present in cytosolic
(probably reflecting monomeric protein) as well as cytoskeletal fractions.
Supplementary References
1. Wikler, K. C. & Rakic, P. Distribution of photoreceptor subtypes in the retina of diurnal and nocturnal
primates. J. Neurosci. 10, 3390-3401 (1990).
2. Ahnelt, P. K., Moutairou, K., Glösmann, M. & Kübber-Heiss, A. Lack of S-opsin expression in the brush-
tailed porcupine (Atherurus africanus) and other mammals. Is the evolutionary persistence of S-cones a
paradox? In Normal and Defective Colour Vision (eds Mollon J. D. et al.), pp. 31-38. (Oxford University
Press, 2003).
3. Müller, B., Goodman, S. M. & Peichl, L. Cone photoreceptor diversity in the retinas of fruit bats
(Megachiroptera). Brain Behav. Evol. 70, 90-104 (2007).
4. Jacobs, G. H. & Deegan II, J. F. Cone photopigments in nocturnal and diurnal procyonids. J. Comp. Physiol.
A 171, 351-358 (1992).
5. Peichl, L. & Pohl, B. Cone types and cone/rod ratios in the crab-eating raccoon and coati (Procyonidae).
Invest. Ophthalmol. Vis. Sci. 41, 494, Abstract no. 2630 (2000).
6. Peichl, L., Behrmann, G. & Kröger, R. H. For whales and seals the ocean is not blue: a visual pigment loss
in marine mammals. Europ. J. Neurosci. 13, 1520-1528 (2001).
7. Peichl, L. & Moutairou, K. Absence of short-wavelength sensitive cones in the retinae of seals (Carnivora)
and African giant rats (Rodentia). Europ. J. Neurosci. 10, 2586-2594 (1998).
8. Crognale, M. A., Levenson, D. H., Ponganis, P.P., Deegan II, J. F. & Jacobs, G. H. Cone spectral sensitivity
in the harbor seal (Phoca vitulina) and implications for color vision. Can. J. Zool. 76, 2114-2118 (1998).
9. Meredith, R. W., Gatesy, J., Emerling, C. A., York, V. M. & Springer, M. S. Rod monochromacy and the
coevolution of Cetacean retinal opsins. PLoS Genetics 9(4), e1003432 (2013).
10. Levenson, D. H. & Dizon, A. Genetic evidence for the ancestral loss of short-wavelength-sensitive cone
pigments in mysticete and odontocete cetaceans. Proc. R. Soc. Lond. B 270, 673679 (2003).
11. Nyakatura, K. & Bininda-Emonds, O. R. P. Updating the evolutionary history of Carnivora (Mammalia): a
new species-level supertree complete with divergence time estimates. BMC Biology 10, 12 (2012).
ResearchGate has not been able to resolve any citations for this publication.
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Most terrestrial mammals have colour vision based on two spectrally different visual pigments located in two types of retinal cone photoreceptors, i.e. they are cone dichromats with long-to-middle-wave-sensitive (commonly green) L-cones and short-wave-sensitive (commonly blue) S-cones. With visual pigment-specific antibodies, we here demonstrate an absence of S-cones in the retinae of all whales and seals studied. The sample includes seven species of toothed whales (Odontoceti) and five species of marine carnivores (eared and earless seals). These marine mammals have only L-cones (cone monochromacy) and hence are essentially colour-blind. For comparison, the study also includes the wolf, ferret and European river otter (Carnivora) as well as the mouflon and pygmy hippopotamus (Artiodactyla), close terrestrial relatives of the seals and whales, respectively. These have a normal complement of S-cones and L-cones. The S-cone loss in marine species from two distant mammalian orders strongly argues for convergent evolution and an adaptive advantage of that trait in the marine visual environment. To us this suggests that the S-cones may have been lost in all whales and seals. However, as the spectral composition of light in clear ocean waters is increasingly blue-shifted with depth, an S-cone loss would seem particularly disadvantageous. We discuss some hypotheses to explain this paradox.
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Most non-primate mammals have two types of cone: short-wavelength sensitive (S) and middle-to-long-wavelength sensitive (M/L) cones. In two species of African giant rats, Cricetomys gambianus and C. emini, and in two species of earless seals, Phoca hispida and P. vitulina, the retinal cone types and cone distributions were assessed with antibodies specific for the M/L-cone opsin and the S-cone opsin, respectively. All four species were found to completely lack S-cones, while M/L-cones were present in low densities. M/L-cone densities, rod densities and cone/rod ratios were determined across the retina. Cone proportions are about 0.3-0. 5% in C. gambianus, 0.5-0.8% in C. emini, and 1.5-1.8% in P. hispida. An absence of S-cones has previously been reported in a few nocturnal mammals. As earless seals are visually active during night and day, we conclude that an absence of S-cones is not exclusively associated with nocturnality. The functional and comparative aspects are discussed.
Article
All mammals ancestrally possessed two types of cone pigments, an arrangement that persists in nearly all contemporary species. However, the absence of one of these cone types, the short-wavelength-sensitive (SWS) cone, has recently been established in several delphinoid cetacean species, indicating that the loss of this pigment type may be widespread among cetaceans. To evaluate the functional condition of SWS cones in cetaceans, partial SWS cone-opsin gene sequences were obtained from nuclear DNA for 16 species representing 12 out of the 14 extant mysticete (baleen) and odontocete (toothed) families. For all these species one or more mutations were identified that indicate that their SWS cone-opsin genes are pseudogenes and thus do not code for functional visual pigment proteins. Parsimonious interpretation of the distribution of some of these mis-sense mutations indicates that the conversion of cetacean SWS coneopsin genes to pseudogenes probably occurred before the divergences of the mysticete and odontocete suborders. Thus, in the absence of dramatic homoplasy, all modern cetaceans lack functional SWS cone visual pigments and, by extension, the visual capacities that such pigments typically support.