Table des matières

This blog is part of our colourful countdown to the holiday season where we’re celebrating the diversity and beauty of the natural world. In this post, Martin Luehrmann of The University of Queensland takes us on a journey through the development of sight through the evolution of fish and early vertebrates.

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 sunshine on your skin. A rainforest then! Again, something’s rustling. 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? 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 slithering closer towards you. You run.

This simple thought experiment may illustrate just how game-changing the development of sight might have been upon its emergence, and it 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. 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, ranging from simple eyespots (e.g., amphipods) to compound eyes, or from pinhole camera style eyes (e.g., in some cephalopods) to lens camera style eyes such as found in birds, mammals and fish.

image1-3
Left: Water flea larva (Daphnia pulex) with flat eye spot (assemblage of light sensitive cells) © Paul Hebert |  Centre: Fossilised eyes of extinct trilobites from the Cambrian period are among the oldest known eyes and the first ever compound eyes © “trilobites also ‘roll up the rim‘” by subarcticmike | Right: Extant Nautilus still have pinhole camera style eyes that lack both a lens and a cornea © Pedro Manuel Martínez from Pixabay

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 a common ancestor to the amoeba-like placozoans and to 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 photosensitive molecule in a photoreceptor cell. Interactions of amino acids at key sites at or near the binding sites of the chromophore influence the wavelength to which the pigment is maximally sensitive. 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 giving rise to photopigments sensitive to different parts of the wavelength spectrum that range from ultraviolet light (UV), as found for example in many insects, birds and some fish, to green and red.

The key to unravelling the ecological functions of colour vision, therefore, lies in revealing and understanding the evolutionary dynamics that underlie the diversification of these colour vision mediating opsin genes; 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.

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 designs and colour vision. 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 (Agnatha), were ancestors to all fish alive today, jawless and jawed (and in fact all vertebrates, terrestrial or aquatic).

Only two groups of jawless fish remain alive today, lampreys and hagfish. As both lampreys and hagfish, as well as all other extant vertebrates, carry the same classes of opsin genes in their genomes, meaning 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.

image4
Lampreys (Petromyzontiformes) are one of only two surviving groups of ancient jawless fishes that are sister taxa to all extant vertebrates © David Herasimtschuk/Freshwaters Illustrated-USFWS from nakaimagazine.com

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 that impacted animal life unevenly, 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 (Actynopterigyii) 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.

Dunkleosteus
Dunkleosteus was a large, predatory representative of the armoured fish (Placoderms), a group of jawed fishes widely distributed across all world oceans in the Age of Fishes during the Devonian period © dinoanimals.com

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 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.

In addition to this, from research looking into the colour vision of Guppies, where the colour sense of female guppies is tuned towards better perceiving the body colourations of their preferred male mates, we learned about possible links between sexual selection and colour vision evolution. Elsewhere, following work studying the many fish species inhabiting the world’s coral reefs, we now understand that some, 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.

image6
Ambon damselfish (Pomacentrus amboinensis) can see ultraviolet light and identify each other using unique UV-reflective facial patterns © Siebeck et al. 2010

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. Current work seeks to identify the relative importance of their UV opsin 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.

image7
Clownfishes, such as the Clown Anemonefish (Amphiprion percula) sport highly UV-reflective patterns, as seen on this individual photographed using a full-spectrum camera setup (left) and a UV-filtered setup © Justin Marshall

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 that 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 this structure enhances light detection in very dim environments, this hypothesis has never actually been tested behaviourally, primarily due to the virtual impossibility of handling deep sea fishes in laboratories.

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 the multi-bank retina may facilitate colour vision under low light conditions in which traditional colour vision ceases to function.

Discover more posts as part of our Colour Countdown series here.


Nilsson 2021, Annual Review of Vision Science, ‘The Diversity of Eyes and Vision’.

Feuda et al. 2012, PNAS, ‘Metazoan opsin evolution reveals a simple route to animal vision’.

Sibert & Norris 2015, PNAS, ‘New Age of Fishes initiated by the Cretaceous-Paleogene mass extinction’.

Collin et al. 2003, Current Biology, ‘Ancient colour vision: multiple opsin genes in the ancestral vertebrates’.

Sandkam et al. 2015, Molecular Ecology, ‘Beauty in the eyes of the beholders: colour vision is tuned to mate preference in the Trinidadian guppy (Poecilia reticulata).

Siebeck et al. 2010, Current Biology, ‘A Species of reef fish that uses ultraviolet patterns for covert face recognition’.

Mitchell et al. 2020, bioRxiv, ‘CRISPR/Cas9-mediated generation of biallelic G0 anemonefish (Amphiprion ocellaris) mutants’.

Mitchell et al. 2021, Genome Biology and Evolution, ‘Molecular evolution of ultraviolet visual opsins and spectral tuning of photoreceptors in Anemonefishes (Amphiprioninae).

de Busserolles et al. 2021, Journal of Experimental Biology, ‘The visual Ecology of Holocentridae, a nocturnal coral reef fish family with a deep-sea-like multibank retina’.


Source link