The basic blueprint of the retina is similar in all mammals (as in all vertebrates). However, in the course of evolution detailed but significant species-specific adaptations have occured in response to specific lifestyles and visual environments. Our comparative studies on mammals belonging to different orders are aimed at showing how flexible the retinal blueprint is. As detailed knowledge about the mammalian retina is mostly based on extensive studies in a few laboratory species, the project not only reflects a fascination with the diversity found in nature, but also provides important controls for the validity of generalized conclusions drawn from studies in the few model systems. The current focus of our studies is on the photoreceptors. Examples are given below. For more details, see our Max Planck Yearbook article 2010 (in German).Diversity of cone propertiesAll mammals have two basic types of photoreceptors. Cones mediate daylight vision and colour vision, rods mediate vision at night and twilight. We study the populations of rods and cones in species with different diel activity patterns (nocturnal, diurnal, crepuscular, arrhythmic) in an attempt to correlate the photoreceptor arrangements with the lifestyle of the animals (Fig. 1). In most species the photoreceptor arrangement and lifestyle match, nocturnal animals have higher rod densities and lower cone densities than diurnal ones. Exceptions are subterranean rodents (e. g., African mole-rats, South American octodontid species) and the European mole, where we found very low rod densities and unexpectedly high cone densities. How this fits to life in their lightless tunnel systems is as yet unexplained.
The retinal processing of colour is based on the presence of several cone types with different spectral sensitivity. Old World primates and humans are trichromats having three types of cones: blue, green and red. Most other mammals are dichromats with two cone types, commonly blue-sensitive and green-sensitive, respectively. With antibodies against the different visual pigments (opsins), the spectral cone types can be identified histologically / immunocytochemically (Fig. 1). This allows to determine the cone arrangements also in species that are not available to physiological or behavioural experiments. We have confirmed the presence of two cone types in many mammals, but also found deviations from this basic pattern. For example, seals and whales lack the blue cones, they only have green cones and rods. Hence these marine animals are cone monochromats and presumably colour blind. The loss of blue cones is particularly suprising as the marine underwater world is predominantly blue.
Fig. 1: Retinal cone populations in different mammals
In flattened retinae, the spectral cone types were immunolabeled with antibodies against the longwave-sensitive (green) cone opsin (green label) and the shortwave-sensitive (blue/UV) cone opsin (magenta label). The dark spaces between the cones are filled by the unstained rods. The nocturnal to crepuscular cat has a much lower cone density than the diurnal degu. The subterranean coruro has a higher cone density than nocturnal surface-dwelling mammals. All three species possess both spectral cone types, with the shortwave cones forming a minority. In contrast, the marine harbour seal has green cones and rods, but no blue cones. All images are at same magnification. Images: Leo Peichl, MPIBR
Most mammals - including humans - cannot see ultraviolet light, because the cornea and lens block the damaging UV components, and because the blue cones are not very sensitive to UV. However, some nocturnal to crepuscular rodents (e. g., mice and rats) were shown to see UV because the sensitivity of their blue cones is shifted to UV and because their eye optics is UV-transparent. It is assumed that in these species there was no evolutionary pressure to block UV, because at low light levels UV would be less damaging to the retina. We have demonstrated UV-sensitive cones in further rodents and in the mole. To our surprise the diurnal degu also had UV vision. For degus, UV vision must offer significant advantages as it is maintained despite high UV exposure. One advantage may be that it allows degus to see as well as smell the urine scent marks they copiously use to mark their territory. Our measurements showed that fresh degu urine reflects maximally in the UV, whereas old dried urine has a high reflectivity in the green part of the spectrum.
A further focus are the photoreceptors of bats (project of Dr. Brigitte Müller). Some older studies had claimed that the retinae of these highly nocturnal animals have only rods and no cones. However, all species we have studied to date possess cones in addition to rods. This provides them with the capability to also see at higher light levels, for example when starting their foraging flights at the beginning of dusk. Some bat species have relatively well-lit daytime roosts, here the cones may also contribute to vision during daytime (e. g., intraspecific interactions and predator detection). In many bat species, we found the two spectral cone types common in mammals and assume the capability of dichromatic colour vision. Interestingly, the shortwave-sensitive cone type of bats is UV- rather than blue-tuned.
Fig. 2: Retinal cone populations in microchiropetan bats and flying foxesImmunolabeling for the cone opsins in flat-mounted retinae of the short-tailed fruit bat (Carollia perspicillata, Phyllostomidae; top) and the Rodrigues flying fox (Pteropus rodriciensis, bottom). Both species have green cones (green label) and UV cones (magenta label). The insets show a short-tailed fruit bat in flight and and Rodrigues flying fox in resting position hanging upside down. Retinal images: Brigitte Müller, MPIBR
Cone visual pigments and thyroid hormone
We are also interested in the molecular mechanisms that determine which opsin is expressed in a given cone. From studies in mice it is known that thyroid hormone plays a crucial role during cone development, but it was assumed that in mature cones the developmentally established 'opsin program' is fixed and needs no further regulation. We could show that this is not the case. In adult mice and rats that had been rendered hypothyroid for several weeks, all cones switched to the production of UV opsin and reduced green opsin production (Fig. 3). After termination of the treatment, hormone levels returned to normal and the cones reverted to the production of their 'regular' opsin - one cone type to green opsin, the other to UV opsin. We conclude that the spectral cone types, which are defined by the opsin they express, are dynamically and reversibly controlled by thyroid hormone throughout life.
Fig. 3: Cone opsins and thyroid hormone
Expression of cone opsins in an adult healthy rat (top) and an adult rat with thyroid hormone deficiency (bottom). The healthy rat has many green cones (green label) and few UV cones (magenta label). The rat with thyroid hormone deficiency expresses UV opsin in all cones and reduces expression of green opsin. Appearing in lighter magenta in the bottom image are cones that contain some green opsin in addition to the dominant UV opsin. Images: Martin Glösmann, MPIBR