The first ever 'eyes' where nothing more than single, light-sensitive cells. How could organs as complex as our eyes possibly have evolved from this? In this article, originally written for and published in the Applied Ecologists Blog, you will get some of the answers, and learn how my colleagues' and my research addresses this very question.
Imagine waking up and the world is black, your eyelids won’t open. You are lying on something soft but prickly. There’s the screech of birds and nearby leaves rustling. Something’s humming, too. Bees perhaps? The smell is earthy. A forest? It’s hot and humid, yet you cannot feel the warmth of sunshine on your skin. A rainforest then! Again, something rustles. Trees? Bushes? But there’s no wind…!? Suddenly your mind starts racing, and you jump to your feet, crouching and listening carefully. "Where am I?" you wonder, "what’s out there?". Helpless. If only you could see…!
Then, suddenly, your eyes pop open. Blindingly bright, squinting, your sight slowly adjusts to the light. In a single instant you know for certain, this is indeed a rainforest, filled with life, and you were just sleeping on the ground, unprotected. Rustling through the undergrowth, though, was not the wind. It was a python the size of a tree, and now it is slithering towards you. You run.
This simple thought experiment may illustrate just how game-changing the development of sight must have been upon its emergence. It also helps understand why vision has proven so successful in the never-ending quest for the survival of the fittest. Of course in real time, the journey from sightless to complex light sensitive organs capable of producing multi-colour, high resolution images, was neither instantaneous nor linear. It was a gradual process, spanning millions of years and, at times, following several different evolutionary paths.
Unfortunately, our understanding of what forces drive the evolution of visual systems and how they do it, remains vague at best; despite intensive research into the origins of vision, the diversity of visual systems found today, and how they serve their owners' vision needs.
Opsin genes hold the key to understanding vision evolution
Cyanobacteria are believed to have been the first living organisms capable of absorbing and utilising light nearly four billion years ago, albeit purely as a source of energy. Over time, and by adapting to its owners’ specific ecological demands, the mechanisms of light perception evolved dramatically, and many, in the form of eyes, have diversified into the myriad different eye types and shapes found among animals today. From simple eyespots, like those found in larvae of the water flea Daphnia, to compound eyes found in insects and crustaceans; from pinhole camera style eyes, such as those seen in the cephalopod Nautilus, to lens camera style eyes like those seen in birds, mammals and fish.
However, the one development that proved perhaps most pivotal to the evolution of animal vision – and colour vision in particular – was one that occurred at the molecular level in genes coding for a diverse group of proteins collectively known as opsins.
Today, opsin proteins are eponymous for a large family of receptors, some of which form the foundation of nearly all extant visual systems. But the earliest forms of those opsin proteins that would eventually evolve to provide animals with the tools to see were most likely not yet sensitive to light at all and would acquire this feature only much later. These opsin progenitors are believed to have arisen in some of the first ever multicellular animal life on earth, in organisms that are ancestors to both the amoeba-like placozoans and jellyfish, ca. 630-720 million years ago during the Ediacaran Eon. When exactly these proteins gained the function to act as light receptors is uncertain. But it was this functional expansion of opsins, from membrane-bound ion-channels and proton pumps to receptors, that heralded the advent of colour vision.
Bound to a vitamin A-like chromophore, opsins form the photopigment, that is the light-sensitive unit in a photoreceptor cell. Interactions of amino acids at key sites at or near the binding sites of the chromophore influence the wavelength (i.e., the colour of the light) to which the pigment is maximally sensitive. Amino acid changes at such sites, over time and presumably largely due to adaptation, have resulted in a remarkable diversity of genes coding for functionally different versions of opsins and gave rise to photopigments that are sensitive to different parts of the wavelength spectrum, ranging from ultraviolet light (UV), as found for example in many insects, birds and some fish, to the far more common green and red.
The key to unravelling the forces that drive vision evolution, and specifically the diversification of the ability to perceive different colours, therefore lies in revealing and understanding the evolutionary dynamics that underlie the diversification of these colour vision mediating opsin genes; that is their rise and fall, their phylogeny, and base pair changes on the gene level that result in amino acid substitutions that cause colour sensitivity shifts in the visual pigment.
What fish eyes can tell us about the evolution of vertebrate vision
One animal group receiving much attention in this undertaking - and specifically to understand the evolution and behavioural implications of colour vision in vertebrates - are fish. Fish just so happen to represent the largest and most diverse group of all vertebrates. They also display a remarkable diversity in lifestyles, corresponding to different eye and colour vision setups. However, the functions, i.e., the evolutionary drivers, for most of these visual adaptations remain elusive.
The general opsin repertoire common to all vertebrates can be traced back to the Cambrian period ca. 480-540 million years ago, following the Cambrian explosion and the appearance of the first fish. These fish, known as Jawless fish, were ancestors to all fish alive today, jawless and jawed (and in fact all vertebrates, terrestrial and aquatic).
Only two groups of jawless fish remain alive today, lampreys and hagfish. As lampreys and hagfish, as well as all other extant vertebrates, carry the same classes of opsin genes in their genomes, we know that this same set of genes must have been inherited by all descendant groups from a common ancestor. This then suggests that these gene classes already existed prior to the divergence of jawed fishes from jawless fishes during the Silurian period ca. 420-440 million years ago. In other words, vertebrate colour vision as we can observe it today, has had at least 400+ million years of evolution at its disposal to mix, match, and tweak opsin genes to best fit its needs.
During this time, jawed fishes experienced several periods of rapid explosive radiation, coinciding with marked acceleration of molecular evolution. Often this was made possible by mass extinctions which impacted animal life unevenly, thus causing extinction of entire clades while others prevailed. This in turn resulted in swathes of unoccupied ecological niches which fish species alive at the time happily occupied.
Notable such periods include the Devonian, ca. 360-420 million years ago, during which the now extinct armoured fish (Placoderms), such as Dunkleosteus, successfully colonised all global oceans, and is thus fittingly labelled The Age of Fishes. Another, also known as the New Age of Fishes, followed the ‘Dinosaur-killing’ Cretaceous-Paleogene (K-Pg) extinction ca. 66 million years ago. In its aftermath, Ray-finned fishes (the vast majority of all fishes alive today) ascended to their current dominant ecological role. As a consequence, the challenge of unravelling fish colour vision spans thousands of species and virtually all aquatic habitats on earth, from mountain lakes to the deep sea, and from tiny ponds to open oceans.
But, we do not remain entirely in the dark, as some mysteries have indeed been solved. For example, we now know that overall fish colour vision is broadly tuned towards the colours of the environmental light available in each species’ habitat. Deep sea fish colour vision, for instance, is centered around bluer and dimmer light, whereas species inhabiting rivers or lakes, which tend to be tinted yellow or brownish from terrestrial organic matter such as detritus, are more tuned towards those longer wavelengths.
Also, from research looking into the colour vision of Guppies, we learned about possible links between sexual selection and colour vision evolution. In these small, brightly coloured fish that live in tropical lakes and rivers, the colour sense of the females is tuned towards better perceiving the body colourations of their preferred male mates.
Elsewhere, following work studying the many fish species inhabiting the world’s coral reefs, we now understand that some fish, such as the Ambon Damselfish (Pomacentrus amboinensis), whose eyes, unlike those of humans, are highly sensitive to ultraviolet light, thanks to a UV-specific opsin, use this ability to recognise their peers via UV facial patterns.
In our research group, based at the University of Queensland in Brisbane, Australia, we seek to deepen our understanding of these mechanisms by studying opsin evolution and function in coral reef fishes. Among others, our focus species include Anemonefishes (Amphiprioninae), better known as Clownfishes, and Soldier- and Squirrelfishes (Holocentridae).
Anemonefishes can see ultraviolet light, and the white patterns on their bodies heavily reflect these wavelengths. This suggests that for Clownfish, much like for the Ambon damselfish, the ability to see UV-light could be essential for conspecific communication. Currently ongoing experiments seek to identify the relative importance of these fishes' UV opsins in such behaviours by comparing the visual performance of wild-type clownfish with those of lab-reared individuals in which the UV opsin gene has been inactivated via gene editing.
Soldier- and Squirrelfishes are two nocturnally active reef fish families whose ancestors lived in the deep sea. Despite them living on shallow and colourful coral reefs, we recently found that these fishes show visual system features which are otherwise only known from deep sea fishes, for example, a multi-bank retina (multiple layers of photoreceptors in the back of the eye). While it is hypothesized that these structures enhances light detection in very dim environments, this has never actually been tested behaviourally, primarily owing to the virtual impossibility of handling deep sea fishes in aquaria.
Having found this same feature in readily accessible, shallow water reef fishes, now allows us to test behaviourally not only whether Holocentrids are more light sensitive than non-multibank species, but also whether, perhaps, the multi-bank retina may facilitate colour vision under low-light conditions in which traditional colour vision ceases to function.
This way, perhaps one day, we will truly understand why eyes have evolved in exactly the ways they have.
An earlier version of this article was first published on appliedecologistsblog.com and can be accessed here.
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