Australasian Science Magazine

A fossil compound eye, around 515 million years old, from the Emu Bay Shale on Kangaroo Island, South Australia. The individual lenses would have numbered over 3000, with the largest in the centre forming a light-sensitive “bright zone”. Image credit: John Paterson

By Michael Lee & John Paterson

The discovery of exquisite fossils on Kangaroo Island reveal that complex eyes evolved very rapidly during evolution’s Big Bang, the Cambrian explosion, half a billion years ago.

Soon after he presented overwhelming evidence for evolution by natural selection in On the Origin of Species, Charles Darwin confided in a letter to a close colleague: “The eye, to this day, gives me a cold shudder”. He was concerned whether such a complex, integrated organ as the eye could have evolved in incremental steps by random mutation and blind natural selection.

He need not have worried: there are examples of animals living today showing virtually all stages in eye evolution, from those with nothing more than a tiny, single light-sensitive cell to those with large, intricate eyeballs.

Sophisticated eyes capable of forming images have evolved more than 50 times in the animal kingdom, and simulation studies have shown that they can evolve very rapidly indeed. In fact, it has been suggested that a fairly simple focused lens eye can evolve within only a few hundred thousand years – a geological blink in time.

However, when it comes to the fossil record, Darwin’s dilemma was well-founded: the eyes of most animals are constructed of soft tissue that doesn’t fossilise well, although there are some notable exceptions. For instance, trilobites have so much armour that even their eye surfaces are hardened, so we can infer trilobite vision in very fine detail. Similarly, many reptiles and birds have a ring of tiny bones around the eye, called the sclerotic ossicles, allowing us to reconstruct the shape of their eyeballs.

From these fossils, we know that certain trilobites, dinosaurs and ichthyosaurs had eyes adapted to see in dim light. However, we have little information for much of the rest of the animal kingdom.

This apparent paucity of eyes, or at least lack of optical details, in the fossil record has been exasperating because the evolution of sharp vision has been suggested as a trigger for arguably the greatest event in evolution after the origin of life. Virtually all living animal body plans burst into existence between 540 and 520 million years ago in an evolutionary “Big Bang” called the Cambrian explosion. Arthropods, molluscs, echinoderms, annelids, chordates (including vertebrates) and many other groups appear at this time and have largely kept their body plans intact until the present.

Such a striking evolutionary event suggests an unusual trigger. One hypothesis, most cogently presented in Andrew Parker’s book In the Blink of an Eye, is that the origin and evolution of good vision played an integral part. Before the Cambrian there was virtually no predation and little movement: it was a very slow and lazy world. Evolution of sharp eyesight would have allowed creatures to actively search for food, kick-starting the evolution of the first predators. This in turn could have triggered a rapid evolutionary arms race, with predators and prey evolving adaptations (e.g. chewing mouthparts), counter-adaptations (e.g. armour) and novel behaviours (e.g. swimming, burrowing) to either find food or avoid being eaten.

Parker’s “light switch” theory predicts that many of the earliest Cambrian animals should have sharp vision, but until recently the fossil record has been frustratingly silent on this aspect of early animal evolution. The trilobites of that age had rather simple eyes, while the squishy/soft eyes of other animals were too poorly preserved to infer much at all.

However, exquisite fossils from South Australia have shed new light on the sensory biology of the early Cambrian. The fossils hail from the 515-million-year-old Emu Bay Shale on Kangaroo Island, a short hop across the water from Adelaide.

The first discovery was almost an accident: Jim Jago, a member of our team, was examining a slab of rock collected because it contained a moulting trilobite (trilobites, like insects and crustaceans, shed their exoskeletons as they grew). Near the trilobite he noticed a tiny purplish blob. While it superficially resembled a plate from an armoured Cambrian “worm” called a lobopodian, it was orders of magnitude too big, and the hexagonal arrangement of facets was much too regular. Under the microscope it was clearly part of a perfectly preserved “compound eye”.

Compound eyes are characteristic of arthropods – animals with hard exoskeletons and jointed limbs, such as insects, crustaceans and trilobites. They consist of a curved visual surface covered in dozens, hundreds or even thousands of tiny individual lenses. Arthropods see their world as pixels, with each lens producing a pixel of vision. More lenses mean there are more pixels and better visual resolution. Contrary to the myth perpetuated by Hollywood, each lens does not form a separate image – it would be rather pointless to see the same thing repeated hundreds of times.

We then found five more such eyes in the Emu Bay Shale over the ensuing years. These eyes are much larger and more powerful than the only other well-preserved eyes from the early Cambrian, which are tiny eyes from Chinese trilobites. These trilobites had fewer than 100 lenses in each eye, and would have seen a very blurry world: they could probably detect day and night, and movement, but little else. In contrast, the Emu Bay Shale eyes have over 3000 lenses, and would have been able to detect friend from foe, and survey the general topography of the environment.

Such visual resolution is as good as or even better than many living animals. For instance, the horseshoe crab sees the world with 1000 pixels. Acute vision would have been extremely useful in the fast-paced, dangerous Cambrian oceans.

Because the specimens show signs of wrinkling and tearing, we know that the fossil eyes were originally composed of flexible chitin, which makes up modern arthropod exoskeletons (including the outer layer of their eyes, the cornea). However, during the early stages of fossilisation, the chitin has been replaced with a compound called calcium phosphate, therefore causing the eyes to become mineralised and resistant to decay. This explains why we have found them as fossils, as chitin is rarely preserved.

Disappointingly, we don’t know the exact owner of the eye: all fossils were found isolated, and we suspect might represent moulted corneas (when shedding their “skins”, arthropods cast off the outer layer of their eyes, along with the rest of their exoskeleton). So you can think of our discovery as an unfinished Cinderella story – we’ve found the “slipper”, and now we just need to find the owner! The optical design of these eyes points to an active, highly mobile predator capable of seeing in low light conditions.

These fossils confirm what many had long suspected: that vision (along with many other traits) evolved very rapidly during the Cambrian explosion. The fossils suggest that the evolution of sharp vision either directly helped drive this great event, or at least went along for the ride.

Apart from these eyes, the rocks of the Emu Bay Shale – once mud at the bottom of an ancient seafloor – preserve a diverse array of more than 50 species of marine animals discovered to date, many of which are new to science and await formal description and names. This fossil deposit – the only one of its kind in the Southern Hemisphere – is renowned for not only preserving hard-bodied marine creatures, such as trilobites, but also soft-bodied organisms that are otherwise rare in the fossil record, such as worms. The biota is dominated by arthropods in terms of abundance and diversity, but also consists of sponges, molluscs, worms, brachiopods and a variety of enigmatic forms that currently defy classification within any modern animal group.

In keeping with the exceptional preservation of the eyes, many of the fossil specimens from the Emu Bay Shale also exhibit soft anatomical parts, including antennae, guts, digestive glands and muscle tissue. The mechanisms behind this extraordinary preservation are complex, but one of the major reasons relates to low oxygen levels within the sediment that entombs the organisms, thereby slowing the decay process considerably.

These fossils are gradually revealing more and more of the ancient Cambrian world that our powerful but enigmatic fossil eyes saw in such fine detail.