Section III Biochemical and Physiological Adaptations
Introduction S.N. ARCHER and M.B.A. DJAMGOZ For a sensory system to function optimally, it must be adapted to receiving and responding to specific sets of physical stimuli. If there exists the possibility that the characteristics of the stimulus can change over time, then the sensory system must further adapt to those changes in order to remain functionally expedient. From this type of simple assumption, we can make some basic predictions about the adaptation of a sensory system: I) Where we observe the widest range of stimuli characteristics we should expect to see the greatest adaptation in the sensory system. 2) Where the range of stimulus characteristics, become restricted or specialised, we should expect to see a corresponding focus of sensory system adaptation. 3) If the characteristics of the sensory stimuli are changing over a period of time, then we should expect to find adaptive mechanisms in the sensory system that are able to respond within the same time scale. When John Lythgoe first wrote 'The Ecology of Vision' (1979) he was exploring the natural environment for evidence of correlations between the visual system and the behavioural ecology of an animal. He was essentially documenting examples of where the above predictions were obviously in operation. Many of these examples are found in fish that inhabit a wide diversity of spectral environments and are perhaps presented with the greatest set of spectral stimuli as well as extreme light-limiting conditions. As light fades and becomes monochromatic in the deep sea it is not surprising to discover that many deepliving species shift their spectral sensitivity to match the precious narrow band of penetrating light. Although this correlation is easy to understand, the ecological approach to vision often identifies other mechanisms that are much more subtle components of the complex adaptation. This section of the book looks at how the function of the visual system relates to the ecology of vision and how evolution has been able to work upon biochemical and physiological aspects of function to produce adaptation to the environment. Adaptations of visual pigments to the aquatic environment are discussed in detail by Partridge and Cummings in Chapter 8. This chapter begins by making the important point that past correlations between vision and the environment highlighted by the ecology of vision have been extremely useful in identifying interesting areas for further research but, importantly, have not always addressed specific questions. Thus, it is not enough to observe an interesting correlation but it is also necessary to understand how the particular adaptation benefits the overall biology of the organism. In other words, what evolutionary pressures have been instrumental in selecting the adaptation? For example, S.N. Archer et al. (eds.), Adaptive Mechanisms in the Ecology of Vision, 247-250 1999 Kluwer Academic Publishers. 247
248 although most deep-sea fishes are maximally sensitive to blue light around 480-490 nm, the deep-sea fish Aristostomias tittmanni also has a visual pigment that is maximally sensitive to red light (Partridge & Douglas, 1995). In order to understand this apparent rule-breaking adaptation, it is necessary to know that the fish also emits red bioluminescence and is probably using this visual pigment for a private communication channel. This is an example of the visual system focusing on a specialised stimulus. But, as Partridge and Cummings point out, for an explanation such as this to be without doubt we must be sure that the adaptation of red sensitivity has been selected in this fish because it confers to the animal the real advantage of a private communication channel. In Chapter 9, Marshall, Kent and Cronin review the visual pigment sensitivity adaptation found in the crustaceans. These animals inhabit a similar variety of niches to fish but have not produced such diversity in visual pigment adaptation. Most crustaceans have only a pair of visual pigments in the UV Iviolet and blue/green regions of the spectrum. These sensitivities are well separated and it is not clear if the pigments interact to provide colour vision. In freshwater crayfish these pigments can become further separated as the sensitivity of the blue/green pigment is pushed up towards the red end of the spectrum. As in fish, this adaptation has been achieved by replacing rhodopsin with porphyropsin pigments (or a variable mixture) and presumably the selection pressure has also been the same (i.e. that freshwater generally transmits more longer wavelength light). In the crustaceans it is not so easy to find precise correlations between spectral sensitivity and environmental light. For many crustaceans the spectral sensitivity of their visual pigments is not exactly matched to the light available for vision (as in deep-sea crustaceans). This may be due to the fact that they have a limited number of visual pigments available and compromises have to be made as regards matching spectral sensitivity to the underwater light spectrum, matching the spectrum at different times, being receptive to bioluminescent light sources or being tuned for species specific behavioural tasks. Within the crustaceans there are probably more examples where the ecology of vision approach identifies correlations that are composed of many subtle elements. Another overriding pressure may come from the requirement to possess polarised light sensitivity. Sensitivity to polarised light could be achieved by the spectral positioning of a visual pigment either side of the polarisation minimum and this could further influence visual pigment adaptation. Lastly, it should be remembered that the crustaceans also give us the most numerous set of visual pigments yet encountered in an organism. The stomatopods can have up to 16 different visual pigments that show a high degree of potential specialisation in function. In these animals, it appears that selection pressure from behaviour has had a large influence in the adaptation of visual pigments. In 'The Ecology of Vision',John Lythgoe emphasized mainly the relevance of photoreceptor/photopigment characteristics to visual ecology. However, the last
249 two decades have seen tremendous advances in our understanding of the postreceptoral neuronal wiring of the vertebrate retina, and how this varies in animals with different visual requirements. Furthermore, we now appreciate that the adult retina is remarkably plastic, especially in lower vertebrates (fish, amphibians), and retinal functional organization can be modified significantly by light/dark adaptational mechanisms with distinct neurochemical control (Wagner and Djamgoz, 1993). The next two chapters (10 and 11) deal with these aspects as regards outer and inner retinal signalling, respectively. Djamgoz, Vallerga and Wagner (Chapter 10) adopt a comparative approach to terrestrial mammals and fish as examples of vertebrates living in markedly different visual environments and review the functional connectivity of photoreceptors, horizontal cells and bipolar cells. Emphasis is placed upon mechanisms of synaptic transfer and spatio - chromatic signalling. The role played by dopamine in mediating light/dark adaptational synaptic plasticity is covered in some detail. Frishman and Robsin (Chapter 11) complement this by a parallel account of the inner retina. In the latter case, however, the mammalian retina is covered in greater detail due to the imbalance in the available information. In fact, much work remains to be done on understanding the functional organization of the inner retinae in fish in relation to visual ecology. As already noted, for a sensory system to remain efficient it must be capable of responding to changing stimuli, some times within the same time scale. In Chapter 12, Beaudet and Hawryshyn describe ontogenetic mechanisms in fish that enable them to adapt their visual systems rapidly in response to the changing light environments that are encountered during migration. Flatfish larvae occupy bright, surface water and have pure-cone retinae with a single visual pigment. When they metamorphose and become bottom dwellers their visual system adapts to more dim light conditions by developing rods and expressing new visual pigments (in addition to a rather spectacular eye migration). Juvenile salmon migrate from the streams where they were hatched to live in ocean water. During this migration they lose a class of photoreceptors from their retinal mosaic that provided them with UV sensitivity. The UV sensitivity must be beneficial to the juveniles in shallow freshwater but is no longer required when they migrate into deeper sea water. As John Lythgoe (1979) pointed out, a cone that contains a non-functional visual pigment is occupying valuable space in the retinal mosaic. Interestingly, there is also evidence that the UV-sensitive pigment may reappear when the adults return to streams to reproduce. An opposite sense of migration occurs in the European eel where mature adults leave freshwater to return to deep-sea breeding grounds. Here the sensitivity of the rod-dominated retina shift from being green to blue sensitive, presumably as an adaptation to deep sea light conditions. In this adaptation the visual pigments of the rod photoreceptors become entirely composed of rhodopsins and a new opsin is introduced that shifts the maximum spectral sensitivity to the blue region of the spectrum. The switch in opsin has been shown to be brought about by a change in opsin
250 gene expression and, because of the high levels of opsin protein turnover in outer segments, this adaptation can occur very rapidly. All these examples clearly demonstrate further that the visual system has a high degree of in-built plasticity. This plasticity provides the visual system of a particular species with the mechanisms to adapt quickly to changes in external stimuli but must also provide the variation upon which selection pressure can drive evolution of the visual system. In the final chapter (13) of this section, Bowmaker and Hunt examine in detail the molecular mechanisms that determine the spectral sensitivity of visual pigments. The visual pigments are the molecular interfaces between the outside environment and the visual system. All visually coded information passes through the visual pigments and an understanding of how they encode the information and transduce photons into electrical signals is essential. The molecular dissection of visual pigments has allowed us to understand how spectral sensitivity can be altered by changing opsin structure. From this we can appreciate how evolutionary selection pressure has been able to adapt visual pigment spectral sensitivity and how plasticity during development can be achieved by changes in opsin gene expression. Knowledge of the molecular biology of visual pigments has also allowed us to determine the molecular basis for our own colour vision deficiencies. References Lythoe, J. N. (1979) The Ecology o/vision. Clarendon Press, Oxford. Partridge, J. C. and Douglas, R. H. (1995) Far-red sensitivity of dragon fish. Nature 375, 21-22. Wagner, H.-J. and Djamgoz, M. B. A. (1993) Spinules: A case for retinal synaptic plasticity. Trends in Neuroscience 16,201-206.