In The Blink Of An Eye

by Andrew Parker

  Many deep-sea animals share the ‘big eye’ characteristic of Bathynomus. Fish, squids and shrimps, to name but a few, have larger, more sensitive eyes in the deep. Evolution has continued to provide adaptations to light here, even though the light is extremely low. Light must really be a powerful stimulus. But I won’t dwell any longer on the adaptation to reduced light found in animals today, partly because some animals produce their own light in the deep sea. Even where light is extremely dim, selective pressures still act on animals to be adapted to light - to see it and even produce their own, although Bathynomus is not one of the light producers. This self-produced light, known as bioluminescence, will be described in Chapter 5. Here it may only complicate matters, although the general light field can still be described as low in the deep sea.

  To get the picture of life in complete darkness we must head for caves. But before leaving the deep sea, I will return to Bathynomus and another lesson it can teach us - that, in contrast to the outcomes described in Chapter 3, the pace of evolution slows in environments with little light.

  Steve Keable set about describing the isopods caught in shallow waters. There were clearly many new species - the contents of the shallow-water traps could be easily sorted into groups based on appearance. Museum volunteers without previous experience of either isopods or taxonomy could carry out this task. There were many obvious characteristics separating species A from species B. Some species had legs covered in spines, some without spines. Some had long antennae, others short antennae. And so on. The identification, and consequently the taxonomy, was straightforward for the shallow water isopods, but enhanced by Steve’s refined taxonomic methods characteristic of the Lowry group.

  To summarise, in shallow water evolution had resulted in many species of isopods, partly in response to the increase in niches created by light. And each species was considerably different - many genetic mutations had taken place over a limited time period, so evolution had been rapid where light levels were high. But how can I talk about time here, when all we have to examine are the species alive today? Surprisingly I can offer some justification. My evidence derives not from the fossil record of isopods - unfortunately that is inadequate. Instead clues can be drawn from the history of the Earth - plate tectonics, as described in Chapter 2.

  The Australian plate is part of the Earth’s crust. It consists of terrestrial land, and the submerged continental shelf and continental slope. The continental shelf inclines gently from the sea shore to a depth of about 200 metres. Then the continental slope commences as the sea floor plunges rapidly towards the Abyssal Plain, another gently sloping part of the sea floor, beginning at about 5,000 metres in depth. The base of the continental slope marks the edge of the Australian plate. So animals living on the sea floor down to depths of at least 1,000 metres are obviously well separated geographically where they occur on different plates. A species could conceivably occupy a large part of one plate, within a range of depths, by circumventing the land. But animals cannot migrate to other plates. They are divided by deep ocean, or forbidden territory. However, as described in Chapter 2, the different plates of today were once joined, but became separated throughout geological time. The consequence of this for animals is that species separated geographically today evolved from ancestors once living together on the same plate. It’s also interesting to point out in this chapter that the Australian, Indian and Mexican plates (or continental slopes) were completely separated 160 million years ago.

  Scavenging isopods were once caught during some early random trapping in Indian and Mexican waters. Steve Keable compared his shallow-water Australian isopods with these species. Just as there were considerable differences between each species within Australia, the scavenging isopods from India and Mexico were very different again. They were all related, in that they belonged to the same small branch of the evolutionary tree, but they had diverged considerably, to adapt to different niches in different light environments. So what can we learn from this?

  The global picture informs of considerable evolution over 160 million years in an environment with substantial sunlight. One hundred and sixty million years ago, a population of ancestral isopods was divided geographically, travelling in different directions on board the continental shelves of three different plates. The ancestral species continued to evolve, but in three different environments. The result is that evolution yielded copious species in each case, but was different each time. Two environments are never the same, and evolution is reflected in this. But remember that here we are dealing with environments where light is present. In contrast, Steve’s clearly defined mission was not to be echoed in Jim Lowry’s task.

  Jim was left with Bathynomus to tackle. At first, this appeared to be a prize project - Bathynomus was a magnificent animal. Then problems started to arise. The Bathynomus collected from each depth range on the Australian plate, beginning at 200 metres, all appeared similar. Those marked differences belonging to the shallow water isopods, obvious even to the inexperienced eye, were simply not there. There were slight differences - some individuals had four spines on a leg where others had five - but were these enough to designate more than one species of Bathynomus in the Australian fauna, and indeed, were there any new species here at all? These questions were at the foundation of Jim’s taxonomic task, and the answers lay with the Bathynomus of India and Mexico.

  Figure 4.3 Simplified schematic section through two of Earth’s plates, showing the submarine landscape between, including their line of separation.

  A ‘species’ can be considered a group of similar individuals that reproduce in their natural environment. The word natural is important - related but different species can sometimes reproduce in an artificial environment, but would not do so under natural conditions. Of course, we could not observe the mating behaviour of Bathynomus at 1,000 metres. But when enough physical characteristics are recognised to reinforce a particular relationship, this can provide evidence towards classification. The characteristics of the other legs of the Australian Bathynomus were consistent with those of the first leg considered. Maybe this was grounds for designating two separate species from Australia. Maybe evolution had been slow in the case of the Australian Bathynomus over the last 160 million years - genetic variation was obviously very limited. It was time now to turn our attention to India and Mexico.

  From fossils, we know that Bathynomus also existed earlier than 160 million years ago. It had travelled on separate plates, diverging from an original supercontinent to the regions that are now Australia, India and Mexico. In other words, it had not evolved from shallow-water isopods independently in all three locations during the past 160 million years. An examination of the Bathynomus caught by fishermen from India and Mexico would inform us what had happened to the ancestor over that 160 million years of living in different, isolated environments.

  The pattern of the shallow-water isopods was not replicated in the deep. The Bathynomus of India and Mexico did not differ greatly from those of Australia - they were almost identical. Almost, but not quite. There was a size difference - although all were huge by isopod standards, exclusive size ranges were identified. These echoed the slight differences in shape such as spine numeration. But quite categorically, Bathynomus showed little variation in shape between species. It lived in deep water with little sunlight . . . and it had hardly evolved at all over 160 million years. Voilà! The evidence we have been looking for, and the point of the whole SEAS story.

  This story paints a picture of what happens in environments with little light compared to those environments with considerable light. But the otherwise x, y, or two-dimensional spatial picture, has a third axis - z. The z axis represents time. And the complete picture is of restricted evolution where light is reduced. Genetic mutations have been diminutive as a result of modest selective pressures - pressures where light is not dominant.

  Just to confirm that light is a major limiting factor here, we can compare the fauna living within the sedim
ent of the sea floor of shallow and deep regions. Below the surface of sediment there is no sunlight. So a very different ecosystem exists there, a system not adapted to light. We have always known that the fauna of shallow water sediment is reasonably diverse, where most species derive from ancestors in the exposed waters above, but ecologists had predicted the opposite for deep-sea sediment. Then, in the 1960s, scientists from the Woods Hole Oceanographic Institution in Massachusetts collected deep-sea sediment samples using newly developed equipment. This technology was capable of collecting more specimens from a given area than ever before. And what it collected was beyond all expectations.

  Although there were fewer individuals in the deep-sea sediment compared with its shallow-water counterpart, the number of species was similar. The diversity of life in deep-sea sediments was equal to that in the shallows. So a diversity of animals can potentially survive in the deep sea, and evolution can be as prolific as in the shallows - temperature and pressure, for instance, are not necessarily limiting to speciation. But where animals are adapted to sunlight, and the light levels fall, then the evolutionary brakes are applied and diversification slows down. The potential niches available diminish drastically. Armed with this clue towards solving the Cambrian enigma, we can leave the deep sea.

  Now that we have adapted our vision and thinking to the dark, we are ready to examine an environment that is in total darkness. Rather than choosing the Abyssal Plain, I will select an environment that is slightly more accessible, and consequently one whose inhabitants are better known. Can we strengthen the message taken from the continental shelf and slope as light is removed from the equation completely? The answer to that question follows.

  Caves

  In his book Colours of Animals, Sir Edward Poulton devoted a certain amount of space to cave animals. He stated unequivocally that animals living in darkness were pale because pigment would not be visible in these situations and so would no longer be of any use to the animals. Poulton strongly favoured what became known as the Darwinian view of colour - that ‘wherever colour is seen, it is due to the favouring influence of natural or sexual selection’. That Darwin carefully chose the words ‘Whenever colour has been modified for some special purpose’ seemed to have been overlooked. So it is not surprising that Poulton extended his argument into environments without light. He suggested that in caves ‘it [pigment] is, therefore, no longer maintained by natural selection, and therefore it disappears’. The second therefore became the subject of great dispute.

  Another biologist of the time, J. T. Cunningham, believed that pigment was produced directly by the action of light on the skin. So he thought cave-dwelling animals were pale coloured because there was no light to stimulate the development of pigment. According to Cunningham, light and pigment were directly related. According to others, light is not the cause of pigmentation; it only puts in motion the machinery produced in the animal by natural selection.

  Today, armed with genetic theory, we understand that Cunningham was wrong. But does the pigment machinery, or rather the process of genetic mutation and new gene deployment, stop working when light is removed? Are the cogs in this colour machine literally solar powered, in that they cease to turn without sunlight? Maybe the pigment machine has a reverse gear, one that is engaged in the absence of light. To uncover the complete story, we too should look into the caves.

  It has been worthwhile examining environments with gradually decreasing levels of light, from the dim night-time of land to the almost complete darkness of the deep sea, if only to compare the communities which inhabit them with those of caves. In caves a similar transition in light levels exists. But here the transition occurs much more rapidly. Light fades away in caves over metres, rather than hundreds of metres as in the sea. And at the end of the journey into many caves, we reach a true, undeviating condition of total darkness on Earth.

  I first became interested in caves when Mike Gray, an arachnologist at the Australian Museum, allowed me to examine his latest find. Mike had recently been underground in the Nularbor Plain of South Australia. Soon after entering the cave, he found himself in total darkness. And the fauna, visible under torchlight, rapidly became less diverse as his journey continued. But Mike found what he was looking for - a spider. More than that, he found a new species of spider. It’s not unusual to find a new species of spider in Australia - Mike’s previous discovery was made in his own garage. But this cave dweller appeared different to his garage specimen, or indeed any other spider living outside caves. It was related to the infamous ‘Sydney funnel web’ which meant it was supposed to have either six or eight ‘eyes’. But with the aid of a microscope it became clear this cave species, just 15 millimetres long, had no eyes.

  The deep-sea animals I had examined were adapted to even the most minuscule quantities of light present in their environment - they had big eyes. The cave spider was denied any light and had given up the evolutionary struggle to see. Its lack of ‘eyes’, nonetheless, was an adaptation to light. But did this ‘eye’ loss take place quickly through time? And how powerful was the selection pressure to lose ‘eyes’ a negative evolutionary response to light? It is difficult to answer these questions taking the cave spider as a model - we know too little about its relatives. But cave fish have been studied more intensively, and we have enough pieces of their puzzle to trace their journey through time, from the open ocean and into caves.

  Sometimes bioluminescence exists in caves as it does in the deep sea - cave animals can produce their own light, like living torches. This, again, makes matters complicated - to begin with, we no longer know the exact light conditions. Bioluminescence may create an effectively continuous light field, or it may be intermittent. The light field may be relatively bright, dim or varied to any extent. Although bioluminescence probably causes a fairly faint light field within the big picture, it is best at this stage to consider just those caves where bioluminescence is absent, where the condition of total darkness is satisfied. Such a situation exists within the marine caves of Mexico.

  Most inhabitants of marine caves today originate directly from their ancestors in the open sea. Either these ancestors now no longer exist, or they have moved into some other extreme environment. For instance, one group of small crustaceans, called remipedes, is virtually confined to cave habitats today, even though their evolutionary origin was in the open sea. They are known as a relict fauna - species derived from groups that were formerly widespread and diverse but now survive exclusively in a cave, possibly, according to Bermudan cave biologist Thomas Iliffe, because of reduced competition or predation. Iliffe found that some remipedes in eastern Atlantic caves look very similar to those in caves of the western Atlantic, and this similarity was not the result of convergence - the evolution of similar bodies to adapt to similar environments. Instead the similarity signalled almost zero evolutionary activity. The caves have been separated geographically for over 100 million years and, as for Bathynomus, very little evolution had taken place in the dark environments. Even closer to the Bathynomus story, isopod crustaceans found living in caves, isolated for over 100 million years, also bore a remarkably close resemblance to each other. In fact this story is echoed in many types of animals. And in most cases the explanation given for their current cave living is the same - that their ancestors once inhabited shallow, open seas but were driven out by competitors and predators among the new faunas that appeared throughout geological time. But the Mexican cave fish can provide more information. They have a very close relative living outside their caves today.

  In the previous chapter we saw how the angelfish employs its silvery surface for reflecting light at its opponents, in the style of Star Wars. But there is another, more widespread function for the silver colour of fishes - to make them disappear.

  In near-surface waters, such as the angelfish’s Amazonian habitat, sunlight exists in the form of a beam like a spotlight, as it does on entry through the Earth’s atmosphere. But below these waters the beam form
ation is broken, and sunlight is scattered in every direction. So here objects are illuminated equally from all directions, and no shadows are cast. A mirror in these waters vanishes from sight because in the mirror one sees only a weak reflection of the environment. The mirror becomes an optical illusion - in the direction of the mirror there appears to be only the background environment, with nothing in the way. In the ocean a silver fish is effectively a mirror. A predator looking directly at a silver-sided, or mirrored fish from below sees only a reflection of the surface. So in the direction of the fish there is . . . no fish! But how can a fish’s skin act as a mirror? After all, it contains no metal. There is another way of strongly reflecting all the colours in sunlight into a beam so that it appears as a very bright white, which we know as silver. We turn to structural colours.

  In Chapter 3 we learnt that a thin film causes colour - structural colour. Also, a stack of thin films was found to provide a relatively brighter colour, by reflecting a greater proportion of sunlight. But the reflector caused strong coloured effects rather than white because the thin films were all of the same thickness, and this thickness determined the wavelength, or colour reflected.

  Now imagine a stack of thin films of different thicknesses. Imagine some that reflect blue light above others, that reflect green above yet others, that in turn reflect red. As sunlight strikes this structure, its blue rays would be reflected from the top layers, leaving the green and red rays to continue along their original path. As these rays meet with the middle layers, the green rays are reflected, leaving only red rays to continue along their path. And finally the red rays meet with the lower layers and they too are reflected. So the combined effect of all the layers is the reflection of blue, green and red rays in the same direction. And blue, green and red combine to form white, or silver (silver is a strongly directional form of white). With more layers of different thicknesses, more colours in the spectrum can be reflected. And this is how the fish skin appears silver - it contains a stack of layers of varying thickness.