Animals live in darkness all over the world. Whether they live in caves, burrows or the ocean abyss, they share many common features such as a lack of coloration and long, slender limbs and antennae. The loss of eyesight is one of the most profound and widely-reported of these. Over 150 years ago, this phenomenon was a source of frustration for Darwin, who could not understand any disadvantage to eyesight and decided the loss of eyes must be ‘attributed wholly to disuse’. Since then, several authors have demonstrated that there is in fact a selective pressure for eye loss: it reduces energy wasted on growing and maintaining such a costly and redundant feature. But how exactly does an animal lose its eyes over time? Many reports of dark-living animals describe gradients of eye loss, indicating that the process is successive and constrained. There have been numerous studies specifically focusing on Astyanax mexicanus, a freshwater fish that has several independently blind cave-dwelling populations. These studies have shown that a change to lens development is responsible for blindness in many cases and that certain genes are implicated again and again in independent cases of eye loss. However, no one has yet objectively studied the series of morphological changes that contribute to eye loss throughout a larger group of animals to determine whether the process is in fact constrained and predictable.

Ilanga laevissima, a shallow-water solariellid snail with fullyformed eyes. Image: Professor Dai Herbert.

In a collaborative study with the Natural History Museum, London, I am studying eye morphology in a family of marine snails called solariellids. They are found globally from the coast to the abyss and have very simple eyes, so they make an excellent model for studying depth-related changes to anatomy. After looking through 109 specimens of 29 species under the microscope, it was clear that many deep-sea species display some form of eye alteration. Several had eyes that were sunken beneath the skin and many lacked pigmented eyes altogether. We examined the eyes of nine shallow and deep water species more closely by embedding them in a plastic resin and cutting them into sections 1.5 µm thick. From the sections we reconstructed digital models of the eyes (see Figure 1) in three dimensions and compared their structure between species.

Even amongst such closely related animals, we found a surprising amount of variation and a wide range of morphological features, many of which were invisible from the outside. Five out of nine species showed clear signs of eye reduction including loss of retinal pigmentation, reduction in size, sinking beneath the skin and degradation of the lens. Most intriguingly, these features did not appear in any particular combinations in different species, indicating that the order of reduction events can be surprisingly variable. For example in some species, the eyes were almost perfectly intact but covered over by skin, and in others they remained at the surface but lacked pigmentation and other important structures. In one case two completely different eye conditions have even evolved within a single genus. There was some evidence for limited constraint—we did not find that the optic nerve was damaged in any of the species examined, for example—but the extent of the variation shown in eye anatomy in different species clearly shows that the process of eye loss is highly plastic. By plotting the evolution of each character (e.g. loss of pigment and lens fragmentation) on a phylogenetic tree, we can conclude that eye reduction has evolved at least five times in solariellids, and that the process of eye loss often differs between these instances.

As eye loss has evolved several times independently, here we are essentially able to examine a naturally replicated evolutionary experiment. Other factors which shape the evolution of animal vision such as habitat, physiological constraints and evolutionary heritage, remain largely similar throughout the study group. Of course, there are almost certainly ecological differences between these species that we cannot account for, as most of these animals are highly inaccessible and few (if any) live observations have ever been made of them. However, the fact that under similar conditions several closely-related snails evolve eye loss very differently, or not at all, is very interesting indeed. The evolution of loss is an intriguing field of study which requires more attention, where modern anatomical techniques can shed much light on historical problems such as eye reduction. By studying the evolution of vision and sensory systems, we can better understand how animals interact with their environment and the evolutionary implications that such study holds.

Fig 1. Tomographic model of the eye of the marine snail Bathymophila diadema, with nerves shown in purple and body outline in brown. Image: Lauren Sumner-Rooney.

Lauren Sumner-Rooney (lsumnerrooney01@qub.ac.uk) won ‘best oral presentation’ at the Postgraduate Conference in Hull. Lauren is a member of the MBA.

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Lauren Sumner-Rooney

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