Fixational Eye Movements in the Earliest Stage of Metazoan Evolution

All known photoreceptor cells adapt to constant light stimuli, fading the retinal image when exposed to an immobile visual scene. Counter strategies are therefore necessary to prevent blindness, and in mammals this is accomplished by fixational eye movements. Cubomedusae occupy a key position for understanding the evolution of complex visual systems and their eyes are assumedly subject to the same adaptive problems as the vertebrate eye, but lack motor control of their visual system. The morphology of the visual system of cubomedusae ensures a constant orientation of the eyes and a clear division of the visual field, but thereby also a constant retinal image when exposed to stationary visual scenes. Here we show that bell contractions used for swimming in the medusae refresh the retinal image in the upper lens eye of Tripedalia cystophora. This strongly suggests that strategies comparable to fixational eye movements have evolved at the earliest metazoan stage to compensate for the intrinsic property of the photoreceptors. Since the timing and amplitude of the rhopalial movements concur with the spatial and temporal resolution of the eye it circumvents the need for post processing in the central nervous system to remove image blur.     

Intergenerational reproductive parasitism in a stingless bee

Insect colonies have been traditionally regarded as closed societies comprised of completely sterile workers ruled over by a single once-mated queen. However, over the past 15 years, microsatellite studies of parentage have revealed that this perception is far from the truth ( Beekman & Oldroyd 2008 ). First, we learned that honey bee queens are far more promiscuous than we had previously imagined ( Estoup et al. 1994 ), with one Apis dorsata queen clocked at over 100 mates ( Wattanachaiyingcharoen et al. 2003 ). Then Oldroyd et al. (1994) reported a honey bee colony from Queensland, where virtually all the males were sons of a single patriline of workers – a clear case of a cheater mutant that promoted intra-colonial reproductive parasitism. Then we learned that both bumble bee colonies ( Lopez-Vaamonde et al. 2004 ) and queenless honey bee colonies ( Nanork et al. 2005, 2007 ) are routinely parasitized by workers from other nests that fly in and lay male-producing eggs that are then reared by the victim colony. There is even evidence that in a thelytokous honey bee population, workers lay female-destined eggs directly into queen cells, thus reincarnating themselves as a queen ( Jordan et al. 2008 ). And let us not forget ants, where microsatellite studies have revealed equally bizarre and totally unexpected phenomena (e.g. Cahan & Keller 2003 ; Pearcy et al. 2004 ; Fournier et al. 2005 ). Now, in this issue, Alves et al. (2009) use microsatellites to provide yet another shocking and completely unexpected revelation about the nefarious goings-on in insect colonies: intergenerational reproductive parasitism by stingless bee workers.     

Eye evolution at high resolution: The neuron as a unit of homology

Based on differences in morphology, photoreceptor-type usage and lens composition it has been proposed that complex eyes have evolved independently many times. The remarkable observation that different eye types rely on a conserved network of genes (including Pax6/eyeless) for their formation has led to the revised proposal that disparate complex eye types have evolved from a shared and simpler prototype. Did this ancestral eye already contain the neural circuitry required for image processing? And what were the evolutionary events that led to the formation of complex visual systems, such as those found in vertebrates and insects? The recent identification of unexpected cell-type homologies between neurons in the vertebrate and Drosophila visual systems has led to two proposed models for the evolution of complex visual systems from a simple prototype. The first, as an extension of the finding that the neurons of the vertebrate retina share homologies with both insect (rhabdomeric) and vertebrate (ciliary) photoreceptor cell types, suggests that the vertebrate retina is a composite structure, made up of neurons that have evolved from two spatially separate ancestral photoreceptor populations. The second model, based largely on the conserved role for the Vsx homeobox genes in photoreceptor-target neuron development, suggests that the last common ancestor of vertebrates and flies already possessed a relatively sophisticated visual system that contained a mixture of rhabdomeric and ciliary photoreceptors as well as their first- and second-order target neurons. The vertebrate retina and fly visual system would have subsequently evolved by elaborating on this ancestral neural circuit. Here we present evidence for these two cell-type homology-based models and discuss their implications.     

Chordate betagamma-crystallins and the evolutionary developmental biology of the vertebrate lens

Several animal lineages, including the vertebrates, have evolved sophisticated eyes with lenses that refract light to generate an image. The nearest invertebrate relatives of the vertebrates, such as the ascidians (sea squirts) and amphioxus, have only basic light detecting organs, leading to the widely-held view that the vertebrate lens is an innovation that evolved in early vertebrates. From an embryological perspective the lens is different from the rest of the eye, in that the eye is primarily of neural origin while the lens derives from a non-neural ectodermal placode which invaginates into the developing eye. How such an organ could have evolved has attracted much speculation. Recently, however, molecular developmental studies of sea squirts have started to suggest a possible evolutionary origin for the lens. First, studies of the Pax, Six, Eya and other gene families have indicated that sea squirts have areas of non-neural ectoderm homologous to placodes, suggesting an origin for the embryological characteristics of the lens. Second, the evolution and regulation of the betagamma-crystallins has been studied. These form one of the key crystallin gene families responsible for the transparency of the lens, and regulatory conservation between the betagamma-crystallin gene in the sea squirt Ciona intestinalis and the vertebrate visual system has been experimentally demonstrated. These data, together with knowledge of the morphological, physiological and gene expression similarities between the C. intestinalis ocellus and vertebrate retina, have led us to propose a hypothesis for the evolution of the vertebrate lens and integrated vertebrate eye via the co-option and combination of ancient gene regulatory networks; one controlling morphogenetic aspects of lens development and one controlling the expression of a gene family responsible for the biophysical properties of the lens, with the components of the retina having evolved from an ancestral photoreceptive organ derived from the anterior central nervous system.     

Using perturbations to identify the brain circuits underlying active vision

The visual and oculomotor systems in the brain have been studied extensively in the primate. Together, they can be regarded as a single brain system that underlies active vision—the normal vision that begins with visual processing in the retina and extends through the brain to the generation of eye movement by the brainstem. The system is probably one of the most thoroughly studied brain systems in the primate, and it offers an ideal opportunity to evaluate the advantages and disadvantages of the series of perturbation techniques that have been used to study it. The perturbations have been critical in moving from correlations between neuronal activity and behaviour closer to a causal relation between neuronal activity and behaviour. The same perturbation techniques have also been used to tease out neuronal circuits that are related to active vision that in turn are driving behaviour. The evolution of perturbation techniques includes ablation of both cortical and subcortical targets, punctate chemical lesions, reversible inactivations, electrical stimulation, and finally the expanding optogenetic techniques. The evolution of perturbation techniques has supported progressively stronger conclusions about what neuronal circuits in the brain underlie active vision and how the circuits themselves might be organized.     

The evolution of visual processing and the construction of seeing systems

This paper is concerned with the evolution of visual mechanisms and the possibility of copying their principles at different levels of sophistication. It is an old question how the complex interaction between eye and brain evolved when each needs the other as a test-bed for successive improvements. I propose that the primitive mechanism for the separation of stationary objects relies on their relative movement against a background, normally caused by the animal's own movement. Apparently insects and many lower animals use little more than this for negotiating through a three-dimensional world, making adequate responses to individual objects which they 'see' without a cortical system or even without a large brain. In the development of higher animals such as birds or man, additional circuits store memories of the forms of objects that have been frequently inspected from all angles or handled. Simple visual systems, however, are tuned to a feature of the world by which objects separate themselves by movement relative to the eye. In making simple artificial visual systems which 'see', as distinct from merely projecting the image, it is more hopeful to copy the 'ambient' vision of lower animals than the cortical systems of birds or mammals.     

Regressive evolution: ontogeny and genetics of cavefish eye rudimentation

Two hypotheses exist to explain ontogenetic eye reduction in Astyanax cave fish: first, after lens induction by the primordial eye cup, the lens plays the role of a central regulator of eye and retina regression or, second, the retina itself is an independent unit of eye development. A comparative study of five blind cave fish populations and their surface sister form was performed to investigate the differences of ontogenetic eye regression between the cave populations during different stages of development. The study revealed that, in addition to the initial formation of smaller primordia, eye regression is also caused during later ontogeny by different relative growth and specific histological characteristics. Whereas the cave fish lens never properly differentiates, the regressive process of the retina is transitorily interrupted by ongoing differentiation. In the newly-discovered Molino cave population, even visual cells with well-organized outer segments develop, which are secondarily reduced at a later ontogenetic stage. This result shows that the retina and lens are independent developmental units within the eye ball. Presumably, the genetic systems responsible for both show independent inheritance, which is also corroborated by hybrids of F ₂-crosses between the cave and surface fish, in which lens and retina development do not correlate. During ontogeny, the eye size differs between the cave populations. In Pachón cave fish, the relatively large eye size correlates with an ancient introgression from a surface population, which may have delayed eye regression.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 287–296.     

Rhodopsin population genetics and local adaptation: variable dim-light vision in sand gobies is illuminated

The visual pigments of fish are thought to be adapted to the variable spectral qualities of aquatic light environments. Most research on the role of natural selection on the evolution of rhodopsins and dim-light vision in fish has focused on variation among species and higher taxa. In this issue, Larmuseau et al. reveal substantial intraspecific sequence variation in RH1 (the rhodopsin gene) in sand gobies ( Pomatoschistus minutus ). Using population genetics and molecular evolution approaches, they detect positive selection on RH1 and find evidence for adaptation to local light conditions.     

Social pleiotropy and the molecular evolution of honey bee vitellogenin

In this issue of Molecular Ecology, Kent et al. (2011) describe the adaptive evolution of honey bee vitellogenin that belongs to a phylogenetically conserved group of egg yolk precursors. This glyco‐lipoprotein leads a double life: it is central to egg production in the reproductive queen caste, and a regulator of social behaviour in the sterile worker caste. Does such social pleiotropy constrain molecular evolution? To the contrary; Kent et al. show that the vitellogenin gene is under strong positive selection in honey bees. Rapid change has taken place in specific protein regions, shedding light on the evolution of novel vitellogenin functions.     

Vision in elasmobranchs and their relatives: 21st century advances

This review identifies a number of exciting new developments in the understanding of vision in cartilaginous fishes that have been made since the turn of the century. These include the results of studies on various aspects of the visual system including eye size, visual fields, eye design and the optical system, retinal topography and spatial resolving power, visual pigments, spectral sensitivity and the potential for colour vision. A number of these studies have covered a broad range of species, thereby providing valuable information on how the visual systems of these fishes are adapted to different environmental conditions. For example, oceanic and deep-sea sharks have the largest eyes amongst elasmobranchs and presumably rely more heavily on vision than coastal and benthic species, while interspecific variation in the ratio of rod and cone photoreceptors, the topographic distribution of the photoreceptors and retinal ganglion cells in the retina and the spatial resolving power of the eye all appear to be closely related to differences in habitat and lifestyle. Multiple, spectrally distinct cone photoreceptor visual pigments have been found in some batoid species, raising the possibility that at least some elasmobranchs are capable of seeing colour, and there is some evidence that multiple cone visual pigments may also be present in holocephalans. In contrast, sharks appear to have only one cone visual pigment. There is evidence that ontogenetic changes in the visual system, such as changes in the spectral transmission properties of the lens, lens shape, focal ratio, visual pigments and spatial resolving power, allow elasmobranchs to adapt to environmental changes imposed by habitat shifts and niche expansion. There are, however, many aspects of vision in these fishes that are not well understood, particularly in the holocephalans. Therefore, this review also serves to highlight and stimulate new research in areas that still require significant attention.     

Cavefish as a model system in evolutionary developmental biology

The Mexican tetra Astyanax mexicanus has many of the favorable attributes that have made the zebrafish a model system in developmental biology. The existence of eyed surface (surface fish) and blind cave (cavefish) dwelling forms in Astyanax also provides an attractive system for studying the evolution of developmental mechanisms. The polarity of evolutionary changes and the environmental conditions leading to the cavefish phenotype are known with certainty, and several different cavefish populations have evolved constructive and regressive changes independently. The constructive changes include enhancement of the feeding apparatus (jaws, taste buds, and teeth) and the mechanosensory system of cranial neuromasts. The homeobox gene Prox 1, which is expressed in the expanded taste buds and cranial neuromasts, is one of the genes involved in the constructive changes in sensory organ development. The regressive changes include loss of pigmentation and eye degeneration. Although adult cavefish lack functional eyes, small eye primordia are formed during embryogenesis, which later arrest in development, degenerate, and sink into the orbit. Apoptosis and lens signaling to other eye parts, such as the cornea, iris, and retina, result in the arrest of eye development and ultimate optic degeneration. Accordingly, an eye with restored cornea, iris, and retinal photoreceptor cells is formed when a surface fish lens is transplanted into a cavefish optic cup, indicating that cavefish optic tissues have conserved the ability to respond to lens signaling. Genetic analysis indicates that multiple genes regulate eye degeneration, and molecular studies suggest that Pax6 may be one of the genes controlling cavefish eye degeneration. Further studies of the Astyanax system will contribute to our understanding of the evolution of developmental mechanisms in vertebrates.     

Genetics of personalities: no simple answers for complex traits

Identifying the genes that underlie phenotypic variation in natural populations, and assessing the consequences of polymorphisms at these loci for individual fitness are major objectives in evolutionary biology. Yet, with the exception of a few success stories, little progress has been made, and our understanding of the link between genotype and phenotype is still in its infancy. For example, although body length in humans is largely genetically determined, with heritability estimates greater than 0.8, massive genome‐wide association studies (GWAS) have only been able to account for a very small proportion of this variation ( Gudbjartsson et al. 2008 ). If it is so difficult to explain the genetics behind relatively ‘simple’ traits, can we envision that it will at all be possible to find genes underlying complex behavioural traits in wild non‐model organisms? Some notable examples suggest that this can indeed be a worthwhile endeavour. Recently, the circadian rhythm gene Clock has been associated with timing of breeding in a wild blue tit population ( Johnsen et al. 2007 ; Liedvogel et al. 2009 ) and the Pgi gene to variation in dispersal and flight endurance in Glanville fritillary butterflies ( Niitepold et al. 2009 ). A promising candidate gene for influencing complex animal personality traits, also known as behavioural syndromes ( Sih et al. 2004 ), is the dopamine receptor D4 (DRD4) gene. Within the last decade, polymorphisms in this gene have been associated with variation in novelty seeking and exploration behaviour in a range of species, from humans to great tits ( Schinka et al. 2002 ; Fidler et al. 2007 ). In this issue, Korsten et al. (2010) attempt to replicate this previously observed association in wild‐living birds, and test for the generality of the association between DRD4 and personality across a number of European great tit populations.     

Modelling contemporary evolution in stickleback

During the past decade, two lines of research have advanced our understanding of micro‐evolution. On the one hand, a number of studies have generated evidence for strong selection on phenotypes ( Kingsolver et al. 2001 ) and the contemporary (sometimes deemed ‘rapid’) evolution of phenotypic traits ( Hendry & Kinnison 1999 ). On the other hand, other studies have sought to identify the genes that underlie ecologically important traits ( Ungerer et al. 2008 ). Over the next decade, micro‐evolutionists might expect considerable progress from the study of contemporary evolution at both the phenotypic and genetic level simultaneously. In this issue of Molecular Ecology, Le Rouzic et al. (2011) present a teaser for this approach. They examined contemporary evolution of an adaptive trait with a well‐studied genetic basis, the number of lateral plates, in threespine stickleback (Gasterosteus aculeatus L.). A time series of 20 years of change for this trait after introduction into a pond in Norway was compared with a similar time series of 12 years following the invasion of a lake in Alaska. Using a modelling approach, the authors then teased apart selection acting upon the phenotype and selection acting on a major effect gene. In both time series, selection was strong and consistent. The models suggested that selection could act directly on the phenotype, or through the gene’s pleiotropic effects.     

North Atlantic marine communities through time

How and why ecological communities change their species membership over time and space is a central issue in ecology and evolution. Phylogeographic approaches based on animal mitochondrial DNA sequences have been important for revealing historical patterns of individual species and can provide qualitative comparisons among species. Exciting new methods, particularly implementing approximate Bayesian computation (ABC – Beaumont et al. 2002 ), now allow model‐based quantitative comparisons among species and permit the probabilistic exploration of alternative community‐level hypotheses (see review by Hickerson et al. 2010 ). In this issue of Molecular Ecology, Ilves et al. (2010) use an ABC approach to bring fresh insights into the well‐studied question of how North Atlantic coastal species contracted and expanded their ranges in response to late Pleistocene/Holocene climate fluctuations.     

Tracing the recombination and colonization history of hybrid species in space and time

Hybrid speciation has long fascinated evolutionary biologists and laymen alike, presumably because it challenges our classical view of evolution as a ‘one‐way street’ leading to strictly tree‐like patterns of ancestry and descent. Homoploid hybrid speciation (HHS) has been a particularly interesting puzzle, as it appears to occur extremely rapidly, perhaps within less than 50 generations ( McCarthy et al. 1995 ; Buerkle et al. 2000 ). Nevertheless, HHS may sometimes involve extended or repeated periods of recombination and gene exchange between populations subject to strong divergent natural selection ( Buerkle & Rieseberg 2008 ). Thus, HHS provides a highly interesting setting for understanding the drivers and tempo of adaptive divergence and speciation in the face of gene flow ( Arnold 2006 ; Rieseberg & Willis 2007 ; Nolte & Tautz 2009). In the present issue of Molecular Ecology, Wang et al. (2011) explore a particularly challenging issue connected to HHS: they attempt to trace the colonization and recombination history of an ancient (several MYA) hybrid species, from admixture and recombination in the ancestral hybrid zone to subsequent range shifts triggered by tectonic events (uplift of the Tibetan plateau) and climatic shifts (Pleistocene ice ages). This work is important because it addresses key issues related to the origin of the standing genetic variation available for adaptive responses (e.g. to climate change) and speciation in temperate species, which are topics of great current interest ( Rieseberg et al. 2003 ; Barrett & Schluter 2008 ; de Carvalho et al. 2010 ).     

The human crystallin gene families

Crystallins are the abundant, long-lived proteins of the eye lens. The major human crystallins belong to two different superfamilies: the small heat-shock proteins (α-crystallins) and the βγ-crystallins. During evolution, other proteins have sometimes been recruited as crystallins to modify the properties of the lens. In the developing human lens, the enzyme betaine-homocysteine methyltransferase serves such a role. Evolutionary modification has also resulted in loss of expression of some human crystallin genes or of specific splice forms. Crystallin organization is essential for lens transparency and mutations; even minor changes to surface residues can cause cataract and loss of vision.     

Differences in lens optical plasticity in two gadoid fishes meeting in the Arctic

Arctic and boreal/temperate species are likely to be evolutionary adapted to different light regimes. Currently, the boreal/temperate Atlantic cod (Gadus morhua) is coexisting with the native polar cod (Boreogadus saida) in the Arctic waters around Svalbard, Norway. Here, we studied light/dark adaptative optical plasticity of their eye lenses by exposing fish to bright light during the polar night. Schlieren photography, high-definition laser scanning and ray tracing were used to determine the optical properties of excised crystalline lenses. Both species have multifocal lenses, an optical adaptation for improved color vision. In polar cod, the optical properties of the lens were independent of light exposure. In the more southern Atlantic cod, the optical properties of the lens changed within hours upon exposure to light, even after months of darkness. Such fast optical adjustment has previously only been shown in a tropical cichlid. During the polar night the Atlantic cod lens seems to be unregulated and dysfunctional since it had an unsuitable focal length and severe spherical aberration. We present a system, to our knowledge unique, for studying visual plasticity on different timescales in relation to evolutionary history and present the first study on the polar cod visual system.