The eye is perhaps one of the best examples of Darwinian evolution. Incremental steps driven by natural selection have led to the evolution of this complex organ from its origin as a simple light-sensitive eye spot.
But what is the precise origin of this organ, specialised for vision, within the animal kingdom? A paper published today in Proceedings of the National Academy of Sciences (PNAS) seeks to address this question by examining an important component of any visual system: the light-detecting photopigment.
Photopigments absorb photons of light, triggering a complex cascade of reactions in the process.
These photopigments comprise a photosensitive chromophore, which is generally derived from vitamin A bound to an opsin protein. The photopigments then sit in the plasma membrane of the photosensitive cell.
Although the precise type of chromophore used may vary, it is the class of opsin that largely dictates how a photopigment will function and the wavelengths of light that are absorbed.
In vertebrates, opsins are broadly divided into two classes:
- visual opsins, which are mostly expressed in the eye and engaged in image-forming tasks
- non-visual opsins, which are found outside the retina with a role in the regulation of biological rhythms (such as sleep, and timing of seasonal breeding in birds).
Lineage
Since the determination of the first opsin sequence nearly 30 years ago, more than 1,000 opsin sequences from all lineages of animals have been sequenced.
Most of these DNA sequences derive from either vertebrates (deuterostomes) or invertebrates (protostomes).
Many studies of the sequences’ molecular composition and functionality in light-detection has enabled insights into the molecular adaptation of vision to diverse light environments.
Opsin gene variation can also be used to construct phylogenies – a hypothesis about the evolutionary history of a taxonomic group – that not only reconstruct the evolution of the eye, but also the evolution of species and the tree of life.
In 2003, our group in the School of Animal Biology at UWA (then largely at the University of Queensand) demonstrated for the first time that the photopigments responsible in vertebrates for colour perception are present in the ancient jawless fishes.
This led to the conclusion that vertebrate colour vision evolved at least 540 million years ago in the Cambrian epoch.
The challenge now is to travel further back in time in order to investigate the origin of the eye itself and other light-detecting sensory systems.
Sequences
The new PNAS study, by Davide Pisani’s group from the Department of Biology at the National University of Ireland, extended the analysis of opsin gene evolution to modern representatives of the neuralia – the collective term for Cnidaria (jellyfish and corals), Ctenophora (comb jellies) and Bilateria (all other animals).
A forte of the group’s study lies in the sheer number of sequences compared (nearly 500 opsins) and the improved phylogenetic methods applied.
The majority of the sequences used have been extracted from databases, but the authors have added new sequences identified in the genomes of five non-bilaterian species (a hydrozoan polyp, a sea anemone, a placozoan, and two species of sponges).
From their reconstructed phylogenetic trees, the authors come to the conclusion that the opsin gene that formed the basis for vision in higher species had its origin in the Placozoa, an early eumetazoan, from a gene duplication that also gave rise to the melatonin gene.
This would place the origin of opsin genes at around 700 million years ago, compared to previous estimates of 600 million years ago.
Two subsequent gene duplications in this ancestral neuralian lineage then gave rise to the three main groups of opsin genes, that are defined as:
- ciliary (C)
- rhabdomeric (R),
- Go-coupled/retinal G protein-coupled receptor (Go/RGR).
These latter terms either reflect the cellular origins of the different photosensitive cells (C and R) that express these pigments in more advanced species or the functionality of the pigments (Go/RGR).
The authors also come to the conclusion that the common ancestor probably did not possess a chromophore binding site and as such was unlikely to be a light-sensitive molecule.
State of origin
Even though the phylogenies are better resolved and the authors provide a more parsimonious pipeline for opsin evolution, there are a number of issues with the new PNAS work that may lead to misinterpretation.
The emphasis of the article is to associate opsin evolutionary change with the origin of the eye and the visual system.
But the lack of an eye in many of the species involved in this study means, by definition, that conclusions relating to vision (image-formation) cannot be accurately made.
The majority of opsin classes fall into C, R, or Go/RGR groupings purely as an artefact of the binomial process of phylogenetics and do not necessarily relate to the original meaning of C and R as ciliary or rhabdomeric photoreceptors.
This is a rather simplistic and outdated nomenclature, especially as opsins from these super-lineages are all found in the ciliary photoreceptors of fishes: a classification based on photopigment function would be more relevant to the origin of pigment genes and the selection pressures involved in their evolution.
Much work is still required, including the analysis of functional (probably non-visual) roles within an ecological context, before a full understanding of photopigment origin and how light-detector cells/organs, including the eye, is achieved.
Despite these concerns, the work presented in this new article is interesting and adds to our knowledge of phylogenetic changes that have occurred within the opsin class as a whole, which ultimately laid the foundation for the evolution of the eye, image-formation and colour vision.