It is beginning to look, therefore, as if active, fast-moving, and at least in some cases intelligent animals opt for the camera-eye.64 So, too, we need to remind ourselves that commonalities of eye structure may lead to convergences in brain structure and the evolution of visual centres, which is at least the case within the mammals.65 Yet, so far as visiting aliens go the story more often looks to the immense cylinder, embedded in the cricket pitch, the hatch slowly opening, a hideous scrabbling before the bug-eyed monster levers itself out and begins its obligatory, laser-cannon-powered destruction of the pavilion. The inspiration for this abrupt interruption of the smooth running of the Home Counties is presumably the alien-like appearance of insects, robotic limbs, and empathy-free compound eyes. Clearly, given the immense success of the arthropods, the compound eye has its advantages. For example, the eyes of some deep-sea crustaceans are remarkably adept at collecting the minute quantities of light available at depth, and do so by employing a sort of fibre-optic system.66 This specialized arrangement has arisen independently in two pelagic groups, specifically a galatheid crab and the euphausiids.67 Not only that, but it now seems likely that the compound eye itself is convergent in the arthropods, evolving independently in a group of crustaceans, the ostracods.68 It is interesting also to note convergent evolution of the compound eye in the sabellid annelids69 and bivalve molluscs70 (Fig. 7.3). In the sabellid annelids this type of eye evidently has evolved independently several times.71 In both these groups the shared convergence seems to reflect, however, a rather different adaptation from
that found in the arthropods; here the compound eyes appear to act as a sophisticated optical alarm.72
Yet it is in the arthropods that the compound eyes are most familiar, ranging as they do from the familiar example of the insects to the calcite lens of the extinct trilobites.73 Trilobite eyes are often claimed to be unique, but in fact they show two interesting convergences. The first is in terms of general organization, and entails a comparison with the eyes of the strepsipteran insects,74 a group that we encountered earlier in the context of their convergently derived gyroscopic halteres. The overall resemblance to trilobite eyes, especially the more advanced type known as schizochroal (see below) is quite striking, but strepsipteran eyes (Fig. 7.1) are not calcitic. An equivalent arrangement, albeit on a smaller scale, is found, however, in a group of echinoderms mentioned above, the brittle-stars. Here, on the upper side of the five arms, there are the characteristic calcitic ossicles that make up the flexible skeleton, but evidently modified for the purposes of vision.75 As in the trilobite lens, the optic axis is parallel to the line of sight, an important feature because the mineral calcite shows strong double refraction. This means that light passing through the crystal at an angle to the optic axis is split into two rays, resulting in the formation of a double image. Along the optic axis of the crystal, however, the rays remain together, so that the transmitted image remains single.76 This convergence in calcitic eyes may extend further because each brittle-star ossicle is composed of a series of lenses, each forming a dome-like structure, which is strongly reminiscent of a trilobite compound eye. Just what the brittle-star 'sees'
is rather conjectural because the nervous system is a diffuse net without a central brain (see note 47), and is therefore reminiscent of the cubozoan jellyfish (see above). Even if images are not perceived, the brittle-star's sensitivity to external stimuli is evident in its ability to avoid predators rapidly and in the striking changes in its colour on a daily cycle.77
Trilobite eyes have also attracted considerable attention because the internal structure of the more advanced type of lens, which is referred to as schizochroal,78 appears to have a double component. Such a configuration, it is claimed, acts to minimize the spherical aberration of the perceived image. Accordingly this lens structure evidently anticipated, by hundreds of millions of years, human technology with its grinding of lenses with the same aim of minimizing such optical distortion of the image.79 Interestingly, a somewhat similar arrangement, again to correct spherical aberration, is found in the calcitic lenses of the brittle-star (note 75). So far as the trilobites are concerned, not everyone, however, is entirely convinced by this elegant story. At least in some cases post-mortem changes, such as recrystal-lization in the eye structure, may provide artefacts of structure that were not present in the living trilobite.80
The magic of being able still to see through the lens of a trilobite81 does not mean that one can necessarily avoid a distorted vision of these extinct animals, but let us return to the relative merits of camera- and compound eyes. Will the alien monsters be bug-eyed, or should we prepare ourselves to return the steady gaze of sentience through an eye like ours? As it happens, more probably the latter. This is because, despite its versatility, the compound eye simply does not match the light-collecting powers of the camera-eye. Apart from the ogre-faced and jumping spiders discussed earlier (pp. 156-157) there seems to be only one exception to the rule that arthropods typically have compound eyes (see also note 73). This concerns the unique eyes of a shrimp belonging to a group known as the mysids.82 As in arthropods, the principal eyes are compound, but embedded in the posterior region of each eye there is an extraordinary addition in the form of a giant lens (Fig. 7.4). In effect the shrimp has evolved a simple eye, consisting of a single enormous lens that overlies a giant crystalline cone. This serves to channel the light to a retina composed of more than a hundred of the individual optical units that are referred to as the rhab-doms. Effectively these rhabdoms, which in the normal compound eye
figure 7.4 The compound eye of a mysid shrimp. Above, entire eye with simple eye located on posterior side. Below, transverse section of eyes. Simple eye is on lower side. (Photographs courtesy of Professor D-E. Nilsson, University of Lund.)
each underlie a separate lens, have been diverted to supply the giant lens. In life the eyes of the shrimp can move freely, and used together the two giant lenses evidently act as a binocular. Looking at this animal changes our perception; as Dan Nilsson and Richard Modlin remark, 'Viewing the live animal from behind ... gives an almost uncanny feeling of being observed'.83
So here in one particular arthropod we have a design that approaches that of our own eyes; yet from the point of view of evolution it appears to be a dead end. As the investigators remark,
The ultimate development is ... a large single facet and crystalline cone supplying light to a common retina of numerous rhabdoms. There can be no further improvement along this line and [the giant eye of this shrimp] has reached the ideal design for a compound eye. Ironically, the ideal compound eye is not really a compound eye at all. It has been turned into a simple eye in order to exploit the advantages of imaging through a single aperture. There is thus little reason for surprise over the unique design in [this shrimp]. It would be more appropriate to wonder why [it] does not share its ingenious solution with other crustaceans or with insects.84
The answer may lie in the difficulties in reorganizing the neural circuitry and, as it happens, with the notable and already noted exception of some spiders (see p. 157), nearly all other arthropods remain stuck with their compound eyes.
In the final analysis camera-eyes are not only different from compound eyes; they are better. This is because in the compound eye the visual array can be increased both by expanding the overall area of the eye and also by the increasingly dense packing of the lens. There are, however, limits to both, and in particular as the lenses shrink in size so their ability to collect enough light to function is compromised. Calculations suggest that if humans were to rely on a compound eye to achieve equivalent vision it would have to be at least a metre across, and more realistically up to 12 metres wide (Fig. 7.5).85 On distant planets there might (or might not) be bug-eyed aliens, but any astronomers are almost certainly going to be equipped with camera-eyes. Perhaps, too, they will have binocular vision, a reasonable enough assumption given its convergent acquisition in birds and mammals.86 Yet, it is also worth remarking here that in a certain
figure 7.5 Why we don't have compound eyes. A conservative estimate of the size of eye a human would require to provide even a near-equivalent of the camera-eye. (Reproduced with permission from Neural principles in vision, edited by F. Zettler and R. Weiler, in the chapter (pp. 354-370) by K. Kirschfeld, fig. 7c; 1996, copyright Springer-Verlag and also with the permission of the author.)
sense the differences between compound and camera-eyes are, at one level, rather superficial. For example, the process of visual tracking in which an animal's coordination of vision and locomotion ensures successful interception of prey (or mate) shows that between humans and such insects as the mantids and hoverflies87 there are 'some remarkable similarities'.88 Not surprisingly, given these similarities, binocular vision has also evolved independently in a number of insects.89 As we shall see later, there are also convergences in the molecular architecture of vision, notably among the proteins known as crystallins and rhodopsins, both of which are essential for any animal eye to work. Moreover, the convergences discussed below in such sensory modalities as olfaction and hearing make it less surprising that there may be parallels in the neural processing of, say, insect and vertebrate eyes.90 The limitations of biological form and the reality of the adaptive framework provide a realistic guide to what there will be 'out there'. Even let us suppose that our extraterrestrial has the inevitable camera-eyes, but these are mounted in little turrets and able to swivel independently. Again we can find a striking convergence here on Earth. Such an arrangement is well known in the chameleon lizards. It entails some remarkable changes to the basic camera-eye. Among the most striking of these is the suppression of the lens and its replacement for refractive purposes by the cornea, which is duly equipped with muscles to effect the changes in shape necessary for focusing. How odd, but this rearrangement is strongly convergent on the eyes of the sand-lances, a group of fish.91 And despite the different media, air as against water, there is a common adaptive explanation. Both chameleons and sand-lances are capable of exceedingly accurate and rapid strikes at their respective prey: in effect the lunging of the entire fish is equivalent to the darting of the chameleon tongue.92
In discussing eyes a number of qualifications are important. First, it is agreed that eyes have evolved independently very many times. In their classic paper Luitfried v. Salvini-Plawen and Ernst Mayr93 write, 'Summing up the different and convergent sequences towards eye perfection in general, there are about 20 or even more independent lines of differentiation including at least 15 cases of independent attainments of photoreceptors with a distinct lens.'94 Although I have emphasized the importance of compound and camera-eyes and their convergences, unique optical configurations do occur. Perhaps the best example is the remarkable eye (or eyes, given that an individual has a whole series distributed along the shell margin) of the scallop, which although camera-like has a system of internal mirrors.95 As Michael Land aptly remarked,96 this represents 'an almost unique example of a type of eye that should exist, but which had not been found until relatively recently'.97 Even so, the reflectivity of the eye depends on the mirror-like properties of the material guanine.98 This compound has already been encountered in the rather different context of providing thin, flexible sheets that would help to gas-proof a Fortean bladder (pp. 112-113). In an optical context, however, not only is guanine found in scallop eyes, but it also forms the reflective structures, known as the tapetum, that are found in the eyes of certain vertebrates, notably deep-sea fish, where they act to concentrate light.99 Nor does its 'optical' use stop there, because the silvery guanine is also widely used as a reflector to channel the light generated by the luminescent organs known as photophores.100
figure 7.6 The optical apparatus of two dinoflagellates, Eiythiopsidinium (left) and Warnowia (right), magnified respectively x460 and x380. Note the bulbous lens and underlying cup. (Reproduced from fig. 1 of Greuet (1968; citation is in note 106), with permission of Urban and Fischer Verlag. (European Journal of Protistology.)
Second, and even more interestingly, eyes are by no means restricted to animals. Most familiar are the various sorts of eye-spot (more strictly light antenna or photosensory apparatus) in the protis-tan eukaryotes such as the single-celled Chlamydomonas or globular colonial Volvox.101 Here, too, independent evolution is widespread,102 and it also turns out that the visual protein (rhodopsin) employed in these eye-spots may be convergent on the equivalent protein found in our eyes and those of other animals (see pp. 171-172). Typically the protistan eye-spot has a reddish or orange colour; this is due to a layer of carotenoids that serve to reflect the incoming light back against the photoreceptor.103 Even so, among the examples of protistan eye-spots, the optical system in the group known as the dinoflagellates is particularly remarkable.104 In this group a variety of eye-spots occur,105 but in certain taxa (e.g. Erythropsidinium and Nematodinium), the organism, which, remember, is a single cell, bears a protruding bulblike structure. In appearance, this is almost telescope-like (Fig. 7.6). Its structure is complex, but in essence it consists of a pigmented cup (melanosome) surmounted by a crystalline lens (or hyalosome)106 which can refract light so that it focuses on the underlying sensitive layer.107 Despite the absence of a nervous system, this tiny optical protuberance, less than a tenth of a millimetre long, is strikingly convergent on the animal eye,108 although most probably it originates from a chloroplast.109 Somewhat nervously, in describing the behaviour of these dinoflagellates, Ester Piccinni and Pietro Omodeo110 remark, 'It is unthinkable that an apparatus of this sort, in spite of the sophistication of its design, can function like an image-forming eye',111 but they speculate that these organisms may detect their prey and
then entangle it with explosively discharged thread-like structures,112 which are also convergent.113
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