Evolution Of Eyes Research Articles

Vertebrate ancient opsin and melanopsin: divergent irradiance detectors

Both vertebrates and invertebrates respond to light by utilising a wide-ranging array of photosensory systems, with diverse photoreceptor organs expressing a characteristic photopigment, itself consisting of an opsin apoprotein linked to a light-sensitive retinoid chromophore based on vitamin A. In the eye, the pigments expressed in both cone and rod photoreceptors have been studied in great depth and mediate contrast perception, measurement of the spectral composition of environmental light, and thus classical image forming vision. By contrast, the molecular basis for non-visual and extraocular photoreception is far less understood; however, two photopigment genes have become the focus of much study, the vertebrate ancient (va) opsin and melanopsin (opn4). In this review, we discuss the history of discovery for each gene, as well as focusing on the evolution, expression profile, functional role and broader physiological significance of each photopigment. Recently, it has been suggested independently by Arendt et al. and Lamb that an ancestral opsin bifurcated in early metazoans and evolved into two quite different photopigments, one expressed in rhabdomeric photoreceptors and the other in ciliary photoreceptors. This interpretation of the evolution of the metazoan eye has provided a powerful framework for understanding photobiological organization. Their proposal, however, does not encompass all current experimental observations that would be consistent with what we term a central "Evolution of Photosensory Opsins with Common Heredity (EPOCH)" hypothesis to explain the complexity of animal photosensory systems. Clearly, many opsin genes (e.g. va opsin) simply do not fit neatly within this scheme. Thus, the review concludes with a discussion of these anomalies and their context regarding the phylogeny of photoreceptor and photopigment development.

Evolution of the third eye: a phylogenetic comparative study of parietal-eye size as an ecophysiological adaptation in Liolaemus lizards

The parietal, or third, eye is a photosensory organ situated in the middle of the skull of many lizards. Despite many hypotheses, its exact ecological functions are still unclear. Studies have compared the presence and absence of a functioning parietal eye, although there are no quantitative studies of parietal-eye traits in relation to ecology, physiology or behaviour. In the present study, we report the first comparative study of relative parietal-eye size in relation to climatic and thermophysiological variables. We studied thirty species of Liolaemus, a genus of South-American lizards inhabiting a range of climatic conditions, but found little evidence for adaptation to thermal environment, in that parietal-eye size did not vary meaningfully with latitude, altitude or any measures of environmental temperature. Neither did it relate to thermophysiology; there was a weak relation to thermal tolerance, although this was partially confounded with body size, which explained 23% of the among-species variance after controlling for within-species variation. The negative results obtained could not be explained by phylogenetic constraints because we found no evidence of phylogenetic inertia. We also observed high intraspecific variation indicating that parietal-eye size may not be under strong selection for accuracy. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101, 870–883.

Gene duplication and the origins of morphological complexity in pancrustacean eyes, a genomic approach

BackgroundDuplication and divergence of genes and genetic networks is hypothesized to be a major driver of the evolution of complexity and novel features. Here, we examine the history of genes and genetic networks in the context of eye evolution by using new approaches to understand patterns of gene duplication during the evolution of metazoan genomes. We hypothesize that 1) genes involved in eye development and phototransduction have duplicated and are retained at higher rates in animal clades that possess more distinct types of optical design; and 2) genes with functional relationships were duplicated and lost together, thereby preserving genetic networks. To test these hypotheses, we examine the rates and patterns of gene duplication and loss evident in 19 metazoan genomes, including that of Daphnia pulex - the first completely sequenced crustacean genome. This is of particular interest because the pancrustaceans (hexapods+crustaceans) have more optical designs than any other major clade of animals, allowing us to test specifically whether the high amount of disparity in pancrustacean eyes is correlated with a higher rate of duplication and retention of vision genes.ResultsUsing protein predictions from 19 metazoan whole-genome projects, we found all members of 23 gene families known to be involved in eye development or phototransduction and deduced their phylogenetic relationships. This allowed us to estimate the number and timing of gene duplication and loss events in these gene families during animal evolution. When comparing duplication/retention rates of these genes, we found that the rate was significantly higher in pancrustaceans than in either vertebrates or non-pancrustacean protostomes. Comparing patterns of co-duplication across Metazoa showed that while these eye-genes co-duplicate at a significantly higher rate than those within a randomly shuffled matrix, many genes with known functional relationships in model organisms did not co-duplicate more often than expected by chance.ConclusionsOverall, and when accounting for factors such as differential rates of whole-genome duplication in different groups, our results are broadly consistent with the hypothesis that genes involved in eye development and phototransduction duplicate at a higher rate in Pancrustacea, the group with the greatest variety of optical designs. The result that these genes have a significantly high number of co-duplications and co-losses could be influenced by shared functions or other unstudied factors such as synteny. Since we did not observe co-duplication/co-loss of genes for all known functional modules (e.g. specific regulatory networks), the interactions among suites of known co-functioning genes (modules) may be plastic at the temporal scale of analysis performed here. Other factors in addition to gene duplication - such as cis-regulation, heterotopy, and co-option - are also likely to be strong factors in the diversification of eye types.

Reconstructing the evolutionary history of the centriole from protein components.

Centrioles are highly conserved structures that fulfil important cellular functions, such as nucleation of cilia and flagella (basal-body function) and organisation of pericentriolar material to form the centrosome. The evolution of these functions can be inferred from the distribution of the molecular components of extant centrioles and centrosomes. Here, we undertake an evolutionary analysis of 53 proteins known either for centriolar association or for involvement in cilia-associated pathologies. By linking protein distribution in 45 diverse eukaryotes with organism biology, we provide molecular evidence to show that basal-body function is ancestral, whereas the presence of the centrosome is specific to the Holozoa. We define an ancestral centriolar inventory of 14 core proteins, Polo-like-kinase, and proteins associated with Bardet-Biedl syndrome (BBS) and Meckel-Gruber syndrome. We show that the BBSome is absent from organisms that produce cilia only for motility, predicting a dominant and ancient role for this complex in sensory function. We also show that the unusual centriole of Caenorhabditis elegans is highly divergent in both protein composition and sequence. Finally, we demonstrate a correlation between the presence of specific centriolar proteins and eye evolution. This correlation is used to predict proteins with functions in the development of ciliary, but not rhabdomeric, eyes.

Lipid second messengers and related enzymes in vertebrate rod outer segments

Rod outer segments (ROSs) are specialized light-sensitive organelles in vertebrate photoreceptor cells. Lipids in ROS are of considerable importance, not only in providing an adequate environment for efficient phototransduction, but also in originating the second messengers involved in signal transduction. ROSs have the ability to adapt the sensitivity and speed of their responses to ever-changing conditions of ambient illumination. A major contributor to this adaptation is the light-driven translocation of key signaling proteins into and out of ROS. The present review shows how generation of the second lipid messengers from phosphatidylcholine, phosphatidic acid, and diacylglycerol is modulated by the different illumination states in the vertebrate retina. Findings suggest that the light-induced translocation of phototransduction proteins influences the enzymatic activities of phospholipase D, lipid phosphate phosphatase, diacylglyceride lipase, and diacylglyceride kinase, all of which are responsible for the generation of the second messenger molecules.

The Tangled Bank: an introduction to evolution

The Tangled Bank: an introduction to evolution

Wide-field motion tuning in nocturnal hawkmoths

Nocturnal hawkmoths are known for impressive visually guided behaviours in dim light, such as hovering while feeding from nectar-bearing flowers. This requires tight visual feedback to estimate and counter relative motion. Discrimination of low velocities, as required for stable hovering flight, is fundamentally limited by spatial resolution, yet in the evolution of eyes for nocturnal vision, maintenance of high spatial acuity compromises absolute sensitivity. To investigate these trade-offs, we compared responses of wide-field motion-sensitive neurons in three species of hawkmoth: Manduca sexta (a crepuscular hoverer), Deilephila elpenor (a fully nocturnal hoverer) and Acherontia atropos (a fully nocturnal hawkmoth that does not hover as it feeds uniquely from honey in bees' nests). We show that despite smaller eyes, the motion pathway of D. elpenor is tuned to higher spatial frequencies and lower temporal frequencies than A. atropos, consistent with D. elpenor's need to detect low velocities for hovering. Acherontia atropos, however, presumably evolved low-light sensitivity without sacrificing temporal acuity. Manduca sexta, active at higher light levels, is tuned to the highest spatial frequencies of the three and temporal frequencies comparable with A. atropos. This yields similar tuning to low velocities as in D. elpenor, but with the advantage of shorter neural delays in processing motion.

The evolution of eyes and visually guided behaviour

The morphology and molecular mechanisms of animal photoreceptor cells and eyes reveal a complex pattern of duplications and co-option of genetic modules, leading to a number of different light-sensitive systems that share many components, in which clear-cut homologies are rare. On the basis of molecular and morphological findings, I discuss the functional requirements for vision and how these have constrained the evolution of eyes. The fact that natural selection on eyes acts through the consequences of visually guided behaviour leads to a concept of task-punctuated evolution, where sensory systems evolve by a sequential acquisition of sensory tasks. I identify four key innovations that, one after the other, paved the way for the evolution of efficient eyes. These innovations are (i) efficient photopigments, (ii) directionality through screening pigment, (iii) photoreceptor membrane folding, and (iv) focusing optics. A corresponding evolutionary sequence is suggested, starting at non-directional monitoring of ambient luminance and leading to comparisons of luminances within a scene, first by a scanning mode and later by parallel spatial channels in imaging eyes.

Eye evolution: common use and independent recruitment of genetic components

Animal eyes can vary in complexity ranging from a single photoreceptor cell shaded by a pigment cell to elaborate arrays of these basic units, which allow image formation in compound eyes of insects or camera-type eyes of vertebrates. The evolution of the eye requires involvement of several distinct components-photoreceptors, screening pigment and genes orchestrating their proper temporal and spatial organization. Analysis of particular genetic and biochemical components shows that many evolutionary processes have participated in eye evolution. Multiple examples of co-option of crystallins, Galpha protein subunits and screening pigments contrast with the conserved role of opsins and a set of transcription factors governing eye development in distantly related animal phyla. The direct regulation of essential photoreceptor genes by these factors suggests that this regulatory relationship might have been already established in the ancestral photoreceptor cell.

The evolution of phototransduction and eyes

Charles Darwin was acutely aware of the need to account for the evolution of ‘organs of extreme perfection’ such as the eye and, in particular, of the importance of demonstrating that numerous gradations in complexity have existed, with each intermediate stage having provided some kind of

The ‘division of labour’ model of eye evolution

The 'division of labour' model of eye evolution is elaborated here. We propose that the evolution of complex, multicellular animal eyes started from a single, multi-functional cell type that existed in metazoan ancestors. This ancient cell type had at least three functions: light detection via a photoreceptive organelle, light shading by means of pigment granules and steering through locomotor cilia. Located around the circumference of swimming ciliated zooplankton larvae, these ancient cells were able to mediate phototaxis in the absence of a nervous system. This precursor then diversified, by cell-type functional segregation, into sister cell types that specialized in different subfunctions, evolving into separate photoreceptor cells, shading pigment cells (SPCs) or ciliated locomotor cells. Photoreceptor sensory cells and ciliated locomotor cells remained interconnected by newly evolving axons, giving rise to an early axonal circuit. In some evolutionary lines, residual functions prevailed in the specialized cell types that mirror the ancient multi-functionality, for instance, SPCs expressing an opsin as well as possessing rhabdomer-like microvilli, vestigial cilia and an axon. Functional segregation of cell types in eye evolution also explains the emergence of more elaborate photosensory-motor axonal circuits, with interneurons relaying the visual information.

The evolution of early vertebrate photoreceptors.

Meeting the challenge of sampling an ancient aquatic landscape by the early vertebrates was crucial to their survival and would establish a retinal bauplan to be used by all subsequent vertebrate descendents. Image-forming eyes were under tremendous selection pressure and the ability to identify suitable prey and detect potential predators was thought to be one of the major drivers of speciation in the Early Cambrian. Based on the fossil record, we know that hagfishes, lampreys, holocephalans, elasmobranchs and lungfishes occupy critical stages in vertebrate evolution, having remained relatively unchanged over hundreds of millions of years. Now using extant representatives of these 'living fossils', we are able to piece together the evolution of vertebrate photoreception. While photoreception in hagfishes appears to be based on light detection and controlling circadian rhythms, rather than image formation, the photoreceptors of lampreys fall into five distinct classes and represent a critical stage in the dichotomy of rods and cones. At least four types of retinal cones sample the visual environment in lampreys mediating photopic (and potentially colour) vision, a sampling strategy retained by lungfishes, some modern teleosts, reptiles and birds. Trichromacy is retained in cartilaginous fishes (at least in batoids and holocephalans), where it is predicted that true scotopic (dim light) vision evolved in the common ancestor of all living gnathostomes. The capacity to discriminate colour and balance the tradeoff between resolution and sensitivity in the early vertebrates was an important driver of eye evolution, where many of the ocular features evolved were retained as vertebrates progressed on to land.

Space-saving advantage of an inverted retina

Vertebrate eyes are of the simple or camera type with a single optical system that creates an image on the retina in the back of the eye. There, the visual information is encoded as nervous signals by photoreceptors, processed by retinal neurons, and then sent to the brain via the optic nerve. Surprisingly at first sight, the retinal neurons are located between the lens and the light-sensitive parts of the photoreceptors. The tissue scatters some light, which leads to loss of light and image blur. The inverted retina has, therefore, long been regarded as inferior. Here, we provide evidence that the inverted retina actually is a superior space-saving solution, especially in small eyes. The inverted retina has most likely facilitated the evolution of image-forming eyes in vertebrates, and it still benefits especially small and highly visual species.

Developmental sources of conservation and variation in the evolution of the primate eye

Conserved developmental programs, such as the order of neurogenesis in the mammalian eye, suggest the presence of useful features for evolutionary stability and variability. The owl monkey, Aotus azarae, has developed a fully nocturnal retina in recent evolution. Description and quantification of cell cycle kinetics show that embryonic cytogenesis is extended in Aotus compared with the diurnal New World monkey Cebus apella. Combined with the conserved mammalian pattern of retinal cell specification, this single change in retinal progenitor cell proliferation can produce the multiple alterations of the nocturnal retina, including coordinated reduction in cone and ganglion cell numbers, increase in rod and rod bipolar numbers, and potentially loss of the fovea.

Evolution of eyes and photoreceptors

Evolution of eyes and photoreceptors

Feathers with Ocular Architecture: Implications for Functional and Evolutionary Similarities of Visual Signals and Receptors

Studies of visual receptors typically assume that only functionally similar structures are relevant to the evolution of complex eyes. This approach ignores growing evidence that different functional classes of organs often share structural and developmental patterns that pertain to biological sameness (deep homology). However, the potential relevance of non-receptor structures to eye evolution remains largely unexplored. An “ocular” feather color mechanism is described whose structural and optical features resemble those of chambered, image-forming eyes to a remarkable degree. These similarities include a laterally expanded, domed light receiving surface similar to that of an eye, an encapsulated spongy tissue mass whose coherent light scattering properties in the human-visible (destructive) and ultraviolet (constructive) wavelength ranges resemble those of cornea and lens, intervening spaces such as those with humors, and a laminar pigmented shelf whose structure and optics resemble a mirrored tapetum lucidum found behind many retinas. Fourier analysis and optical principles indicate that ocular structures adhere to the same light-handling properties regardless of higher function (receptor or signal). The extent to which chambered eyes and ocular feathers have evolved independently is surprisingly equivocal. On the one hand, broad differences in the location, composition, and development of chambered eyes and ocular feather signals suggest convergent evolution on an ocular organization. However, some level of evolutionary parallelism (generative homology) between chambered eyes and ocular feathers is implicated by similarities in constructional materials, tissue development, and signal transduction cascades. Structural, optical, and developmental similarities also occur between more primitive eyes and the colored dermal papillae responsible for avian skin ornamentation. Functional constraints on light-handling requirements, coupled with developmental constraints in high-stress environments on the body surface, may enhance the similar evolutionary outcomes in the different functional setting. Regardless of the mechanistic details, repeated evolution of eye-like structures in different functional settings reveals a biological potential to produce such organs that is much greater than would be inferred from a survey of receptor structures alone.

Toward Developing Models to Study the Disease, Ecology, and Evolution of the Eye in Mollusca*

Several invertebrate systems have been developed to study various aspects of the eye and eye disease including Drosophila, Planaria, Platynereis, and most recently, the cubozoan jellyfish Tripedalia; however, molluscs, the second largest metazoan phylum, so far have been underrepresented in eye research. This is surprising as mollusc systems offer opportunities to study visual processes that may be altered by disease, vision physiology, development of the visual system, behavior, and evolution. Malacologists have labored for over a century as morphologists, systematists, physiologists, and ecologists in order to understand the structural and functional diversity in molluscs at all levels of biological organization. Yet, malacologists have had little opportunity to interact with researchers whose interests are restricted to the biology and development of eyes as model systems as they tend not to publish in the same journals or attend the same meetings. In an effort to highlight the advantages of molluscan eyes as a model system and encourage greater collaboration among researchers, I provide an overview of molluscan eye research from these two perspectives: eye researchers whose interests involve the development, physiology, and disease of the eye and malacologists who study the complete organism in its natural environment. I discuss the developmental and genetic information available for molluscan eyes and the need to place this work in an evolutionary perspective. Finally, I discuss how synergy between these two groups will advance eye research, broaden research in both fields, and aid in developing new molluscan models for eye research.

Introduction to the Symposium “Molluscan Models: Advancing Our Understanding of the Eye”*

Since the time of Darwin, the eye has been a subject of evolutionary and comparative biologists alike who were intrigued by the structural complexity and morphological diversity of eyes in nature. Much of what we know about the eye—development, structure, physiology, and function—has been determined from only a handful of model organisms, specifically the mouse and the fly. One major phylum in particular, the Mollusca, has been underutilized in investigating the evolution and development of the eye. This is surprising as molluscs display a myriad of eye types, such as simple pit eyes without any apparatus to focus images, compound eyes that superficially resemble the eyes of flies, camera-type eyes that are similar to vertebrate eyes, and eyes with mirrors, just to name a few. As a result, molluscan eyes comprise more morphological diversity than seen even in the largest animal phylum, the Arthropoda. With all of this incredible diversity, how do we as researchers determine which mollusc species should be developed as models to study the eye? Serb provides background for eye research using traditional model organisms and how using molluscan species would be advantageous to understanding the eye. She describes the research potential of molluscan species as model organisms and identifies criteria that might be used to develop a molluscan model and the questions molluscan models might address. One application of molluscan models is to study the cellular biology of human eye disease. As many degenerative eye diseases, such as macular degeneration, have been linked to the mis-organization of the cytoskeleton within retinal cells, understanding the control of cytoskeleton organization and its influence on photoreceptor cell changes may lead to prevention and possible cures for some eye diseases. Gray, Kelly, and Robles utilize Octopus bimaculoides Pickford and McConnaughey, 1949 as a model organism to study the molecular controls of cytoskeleton organization in the retina. Their work identifies a cell signaling pathway (Rho GTPase) that mediates cytoskeleton rearrangements. Errors in this pathway may prove to be one of the factors that disrupts cytoskeleton formation, leading to retinal degeneration. After developing one or several molluscan models of the eye, how does one set about understanding this great diversity of eyes and place it in an evolutionary context? One way is to use a comparative approach to identify conserved and variable components of eye morphology, such as lens composition, photoreceptor number and organization, and overall eye shape. These morphological features can provide evidence for functional differences and visual capabilities among species. Several authors in the symposium take this approach. Speiser and Johnsen examine eye morphology in four species of scallop and a closely related spondylid (Spondylus americanus [Hermann, 1781]). They show that scallop eye structure varies among species, and these structural differences affect optical resolution and sensitivity. Further, they provide evidence that actively swimming species (e.g., Amusium balloti [Bernardi 1861]) have better optical resolution than non-swimming species. Speiser and Johnsen provide several new and exciting hypotheses on how the scallop eye performs and how visual requirements may differ between mobile and immobile species. Morton takes a broader perspective and reviews the diversity of noncephalic eye types in the Class Bivalvia. He hypothesizes a possible evolutionary path to create the double retina system in Pectinidae and Laternulidae through the duplication of sensory structures on the pallial folds. Zieger and MeyerRochow review the variation of cephalic gastropod eyes, concentrating on pulmonate species, which are the beststudied eyes in gastropods. They discuss eye anatomy, differences in retinal design, and the visual capabilities of different optical components. Finally, they describe the ultrastructure of “additional” or “accessory” eyes associated with cephalic eyes in several lineages. These data provide

Eye Evolution: The Blurry Beginning

Recent work on the expression of retinal transcription factors and other molecular cues delivers interesting but partly contradictory information on the early phases of eye evolution.

Ultrastructure of pigmented adult eyes in errant polychaetes (Annelida): implications for annelid evolution

The evolution of photoreceptor cells and eyes in Metazoa is far from being resolved, although recent developmental and structural studies have provided strong evidence for a common origin of photoreceptor cells and existence of sister cell types already in early metazoans. These sister cell types are ciliary and rhabdomeric photoreceptor cells, depending on which part of each cell is involved in photoreception proper. However, a crucial point in eye evolution is how the enormous structural diversity of photoreceptor cells and visual systems developed, given the general molecular conservation of the photoreceptor cells. One example of this diversity can be observed in Annelida. Within the polychaetes the errant forms, taxon Aciculata, constitute the only group possessing true multicellular eyes in the adult stage. Thus far these organs have been investigated only in taxa of Phyllodocida, a subgroup of Aciculata. Data on Eunicida and Amphinomida as well as certain phyllodocidan taxa had been lacking. The ultrastructure of these adult eyes was investigated in various species of errant polychaetes, belonging to Amphinomidae, Eunicidae and Hesionidae, to elucidate whether they provide any phylogenetic clues regarding either the evolution of visual systems in Annelida or lophotrochozoan phylogeny in general. These eyes are composed of numerous supportive pigment cells and rhabdomeric photoreceptor cells and sometimes additional cell types. As a rule the pigment and rhabdomeric cell types form a continuous epithelium in which the two types intermingle. Presence of granules with shading pigment in sensory cells is a common feature but is apparently restricted to a taxon comprising Phyllodocida and Eunicida s. str. Very likely a lens-like structure does not belong to the ground pattern of annelid eyes, despite its presence in Phyllodocida. These lens-like structures are formed by secretions or cellular processes of the pigment cells. In many species the eye cup communicates with the exterior via a small cuticularized canal. This canal is interpreted as a rudiment due to the mode of formation in the epidermis. With respect to current phylogenetic hypotheses, these multicellular eyes have either been developed in the stem species of a taxon Aciculata nested within the polychaetes or have been evolved in the stem lineage of Annelida. Similarities to gastropod eyes are interpreted as convergent and not as indication of common origin. Except for the photoreceptor cells proper, the structure of the adult eyes in polychaetes most likely does not help to resolve lophotrochozoan phylogeny.