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The arthropod compound eye represents one of two major eye types in the animal kingdom and has served as an essential experimental paradigm for defining fundamental mechanisms underlying sensory organ formation, function, and maintenance. One of the most distinguishing features of the compound eye is the highly regular array of lens facets that define individual eye (ommatidial) units. These lens facets are produced by a deeply conserved quartet of cuticle-secreting cells, called Semper cells (SCs). Also widely known as cone cells, SCs were originally identified for their secretion of the dioptric system, i.e. the corneal lens and underlying crystalline cones. Additionally, SCs are now known to execute a diversity of patterning and glial functions in compound eye development and maintenance. Here, we present an integrated account of our current knowledge of SC multifunctionality in the Drosophila compound eye, highlighting emerging gene regulatory modules that may drive the diverse roles for these cells. Drawing comparisons with other deeply conserved retinal glia in the vertebrate single lens eye, this discussion speaks to glial cell origins and opens new avenues for understanding sensory system support programs.

Nautilus is the sole surviving externally shelled cephalopod from the Palaeozoic. It is unique within cephalopod genealogy and critical to understanding the evolutionary novelties of cephalopods. Here, we present a complete Nautilus pompilius genome as a fundamental genomic reference on cephalopod innovations, such as the pinhole eye and biomineralization. Nautilus shows a compact, minimalist genome with few encoding genes and slow evolutionary rates in both non-coding and coding regions among known cephalopods. Importantly, multiple genomic innovations including gene losses, independent contraction and expansion of specific gene families and their associated regulatory networks likely moulded the evolution of the nautilus pinhole eye. The conserved molluscan biomineralization toolkit and lineage-specific repetitive low-complexity domains are essential to the construction of the nautilus shell. The nautilus genome constitutes a valuable resource for reconstructing the evolutionary scenarios and genomic innovations that shape the extant cephalopods., Nautilus, the sole surviving externally shelled cephalopod from the Palaeozoic, holds an important phylogenetic position to understand the evolution of cephalopods. A complete genome of Nautilus pompilius sheds light on the evolution of the pinhole eye and biomineralization.

Morphologically diverse eyes have evolved numerous times, yet little is known about how eye gain and loss is related to photic environment. The pteriomorphian bivalves (e.g., oysters, scallops, and ark clams), with a remarkable range of photoreceptor organs and ecologies, are a suitable system to investigate the association between eye evolution and ecological shifts. The present phylogenetic framework was based on amino acid sequences from transcriptome datasets and nucleotide sequences of five additional genes. In total, 197 species comprising 22 families from all five pteriomorphian orders were examined, representing the greatest taxonomic sampling to date. Morphological data were acquired for 162 species and lifestyles were compiled from the literature for all 197 species. Photoreceptor organs occur in 11 families and have arisen exclusively in epifaunal lineages, that is, living above the substrate, at least five times independently. Models for trait evolution consistently recovered higher rates of loss over gain. Transitions to crevice-dwelling habit appear associated with convergent gains of eyespots in epifaunal lineages. Once photoreceptor organs have arisen, multiple losses occurred in lineages that shift to burrowing lifestyles and deep-sea habitats. The observed patterns suggest that eye evolution in pteriomorphians might have evolved in association with light-guided behaviors, such as phototaxis, body posture, and alarm responses.

Most animals are visually oriented, and their eyes provide their 'window to the world'. Eye size correlates positively with visual performance, because larger eyes can house larger pupils that increase photon catch and contrast discrimination, particularly under dim light, which have positive effects on behaviours that enhance fitness, including predator avoidance and foraging. Recent studies have linked predation risk to selection for larger eyes and pupils, and such changes should be of importance for the majority of teleost fishes as they have a pupil that is fixed in size (eyes lack a pupillary sphincter muscle) and, hence, do not respond to changes in light conditions. Here, we quantify eye and pupil size of individual crucian carp, a common freshwater fish, following controlled manipulations of perceived predation risk (presence/absence). We also tested if crucian carp responded to increased predation risk by shifts in diel activity patterns. We found that crucian carp show phenotypic plasticity with regards to pupil size, but not eye size, as pupil size increased when exposed to predators (pike). Predator-exposed crucian carp also shifted from diurnal to nocturnal activity. Using a modelling exercise, we moreover show that the plastically enlarged pupils significantly increase visual range, especially for small objects under dim light conditions. Overall, our results provide compelling evidence for predator-induced pupil enlargement resulting in enhanced visual capabilities in a teleost fish. Pupil size plasticity in combination with the observed shift towards nocturnal activity may allow for efficient foraging also under dark conditions when predation risk from diurnal and visually oriented predators is reduced. The data highlight the powerful role of predation risk for eye development and evolution.

Evolution in similar environments often leads to convergence of behavioral and anatomical traits. A classic example of convergent trait evolution is the reduced traits that characterize many cave animals: reduction or loss of pigmentation and eyes. While these traits have evolved many times, relatively little is known about whether these traits repeatedly evolve through the same or different molecular and developmental mechanisms. The small freshwater fish, Astyanax mexicanus, provides an opportunity to investigate the repeated evolution of cave traits. A. mexicanus exists as two forms, a sighted, surface-dwelling form and at least 29 populations of a blind, cave-dwelling form that initially develops eyes that subsequently degenerate. We compared eye morphology and the expression of eye regulatory genes in developing surface fish and two independently evolved cavefish populations, Pachón and Molino. We found that many of the previously described molecular and morphological alterations that occur during eye development in Pachón cavefish are also found in Molino cavefish. However, for many of these traits, the Molino cavefish have a less severe phenotype than Pachón cavefish. Further, cave-cave hybrid fish have larger eyes and lenses during early development compared with fish from either parental population, suggesting that some different changes underlie eye loss in these two populations. Together, these data support the hypothesis that these two cavefish populations evolved eye loss independently, yet through some of the same developmental and molecular mechanisms.

The eyes of insects display an incredible diversity of adaptations to enhance vision across the gamut of light levels that they experience. One commonly studied contrast is the difference in eye structure between nocturnal and diurnal species, with nocturnal species typically having features that enhance eye sensitivity such as larger eyes, larger eye facets, and larger ocelli. In this study, we compared eye structure between workers of closely related nocturnal and diurnal above ground foraging ant species (Hymenoptera: Formicidae) in four genera (Myrmecocystus, Aphaenogaster, Temnothorax, Veromessor). In all four genera, nocturnal species tend to have little cuticular pigment (pale), while diurnal species are heavily pigmented (dark), hence we could use cuticle coloration as a surrogate for activity pattern. Across three genera (Myrmecocystus, Aphaenogaster, Temnothorax), pale species, as expected for nocturnally active animals, had larger eyes, larger facet diameters, and larger visual spans compared to their dark, more day active congeners. This same pattern occurred for one pale species of Veromessor, but not the other. There were no consistent differences between nocturnal and diurnal species in interommatidial angles and eye parameters both within and among genera. Hence, the evolution of eye features that enhance sensitivity in low light levels do not appear to have consistent correlated effects on features related to visual acuity. A survey across several additional ant genera found numerous other pale species with enlarged eyes, suggesting these traits evolved multiple times within and across genera. We also compared the size of the anterior ocellus in workers of pale versus dark species of Myrmecocystus. In species with larger workers, the anterior ocellus was smaller in pale than in dark species, but this difference mostly disappeared for species with smaller workers. Presence of the anterior ocellus also was size-dependent in the two largest pale species.

The eye color of birds, generally referring to the color of the iris, results from both pigmentation and structural coloration. Avian iris colors exhibit striking interspecific and intraspecific variations that correspond to unique evolutionary and ecological histories. Here, we identified the genetic basis of pearl (white) iris color in domestic pigeons (Columba livia) to explore the largely unknown genetic mechanism underlying the evolution of avian iris coloration. Using a genome-wide association study (GWAS) approach in 92 pigeons, we mapped the pearl iris trait to a 9 kb region containing the facilitative glucose transporter gene SLC2A11B. A nonsense mutation (W49X) leading to a premature stop codon in SLC2A11B was identified as the causal variant. Transcriptome analysis suggested that SLC2A11B loss of function may downregulate the xanthophore-differentiation gene CSF1R and the key pteridine biosynthesis gene GCH1, thus resulting in the pearl iris phenotype. Coalescence and phylogenetic analyses indicated that the mutation originated approximately 5,400 years ago, coinciding with the onset of pigeon domestication, while positive selection was likely associated with artificial breeding. Within Aves, potentially impaired SLC2A11B was found in six species from six distinct lineages, four of which associated with their signature brown or blue eyes and lack of pteridine. Analysis of vertebrate SLC2A11B orthologs revealed relaxed selection in the avian clade, consistent with the scenario that during and after avian divergence from the reptilian ancestor, the SLC2A11B-involved development of dermal chromatophores likely degenerated in the presence of feather coverage. Our findings provide new insight into the mechanism of avian iris color variations and the evolution of pigmentation in vertebrates., Author summary Birds exhibit striking eye color variations, providing a unique angle for understanding avian evolution. Here we identified the genetic basis of the pearl (white) iris color in domestic pigeons (Columba livia) to a nonsense mutation W49X in SLC2A11B via whole genome sequencing and genome-wide association study (GWAS) approaches. SLC2A11B is a gene with known roles in fish pigment cells differentiation and transcriptome analysis indicated that SLC2A11B loss of function may downregulate the xanthophore-differentiation gene CSF1R and the key pteridine biosynthesis gene GCH1, resulting in the pigeon’s pearl iris phenotype. The SLC2A11B variant was estimated to have originated at approximately 5,400 years ago coinciding with the onset of pigeon domestication and was then under positive selection likely associated with artificial breeding. Potentially impaired SLC2A11B was also found in six species from six distinct avian lineages. Analysis of vertebrate SLC2A11B orthologs revealed relaxed selection in the avian clade, consistent with the scenario that the SLC2A11B-involved development of dermal pigment cells likely degenerated in the presence of feather coverage. Our study sheds new light on the largely unknown genetic mechanism underlying the evolution of avian iris color variations.

Vertebrate eye size typically scales hypoallemetrically with body size—as animals grow larger their eyes get relatively smaller. Additionally, eye size is highly variable across species, and such variability often reflects functional adaptations to differences in behavior and/or ecology. The selective pressures underlying the evolution of eye size are especially well studied in birds, mammals, and fishes. However, whether similar scaling rules and selective pressures also underlie the evolution of eye size in amphibians remains enigmatic. Variation in eye size is intimately linked with variation in brain anatomy, as the retina is ontogenetically part of the brain. Eye size may therefore coevolve with brain size. Here we use phylogenetic comparative methods to study interspecific variation in eye volume across 44 species of anurans from 8 families from the Hengduan Mountains, China. We relate this variation to key factors known to impact eye size evolution in other vertebrate taxa such as body mass, habitat use, defense strategy and foraging mobility. We found that also in anurans eyes size scaled hypoallometrically with body mass. However, neither of the behavioral or ecological factors explained any variation in relative eye size in our sample. Whether this is representative for other frog species needs to be clarified. We therefore conclude that eye size in frogs is tightly linked to body mass evolution but that, at least in the species investigated here, none of our tested ecological and behavioral factors have a strong influence on eye size evolution.

Variation in eye size is ubiquitous across taxa. Increased eye size is correlated with improved vision and increased fitness via shifts in behavior. Tests of the drivers of eye size evolution have focused on macroevolutionary studies evaluating the importance of light availability. Predator-induced mortality has recently been identified as a potential driver of eye size variation. Here, we tested the influence of increased predation by the fish predator, the alewife (Alosa pseudoharengus) on eye size evolution in waterfleas (Daphnia ambigua) from lakes in Connecticut. We quantified the relative eye size of Daphnia from lakes with and without alewife using wild-caught and third-generation laboratory reared specimens. This includes comparisons between lakes where alewife are present seasonally (anadromous) or permanently (landlocked). Wild-caught specimens did not differ in eye size across all lakes. However, third-generation lab reared Daphnia from lakes with alewife, irrespective of the form of alewife predation, exhibited significantly larger eyes than Daphnia from lakes without alewife. This genetically based increase in eye size may enhance the ability of Daphnia to detect predators. Alternatively, such shifts in eye size may be an indirect response to Daphnia aggregating at the bottom of lakes. To test these mechanisms, we collected Daphnia as a function of depth and found that eye size differed in Daphnia found at the surface versus the bottom of the water column between anadromous alewife and no alewife lakes. However, we found no evidence of Daphnia aggregating at the bottom of lakes. Such results indicate that the evolution of a larger eye may be explained by a connection between eyes and enhanced survival. We discuss the cause of the lack of concordance in eye size variation between our phenotypic and genetic specimens and the ultimate drivers of eye size.

Every aspect of vision, from the opsin proteins to the eyes and the ways that they serve animal behavior, is incredibly diverse. It is only with an evolutionary perspective that this diversity can be understood and fully appreciated. In this review, I describe and explain the diversity at each level and try to convey an understanding of how the origin of the first opsin some 800 million years ago could initiate the avalanche that produced the astonishing diversity of eyes and vision that we see today. Despite the diversity, many types of photoreceptors, eyes, and visual roles have evolved multiple times independently in different animals, revealing a pattern of eye evolution strictly guided by functional constraints and driven by the evolution of gradually more demanding behaviors. I conclude the review by introducing a novel distinction between active and passive vision that points to uncharted territories in vision research.

The avian eye color, generally referred to the color of the iris, results from both pigments and structural coloration. Avian iris colors exhibit striking interspecific and, in some domestic species, intraspecific variations, suggesting unique evolutionary and ecological histories. Here we tackled the genetic basis of the pearl (white) iris color in domestic pigeons (Columba livia), to elucidate the largely unknown genetic mechanism underlying the evolution of avian iris coloration. Using a genome-wide association study (GWAS) in 92 pigeons, we mapped the pearl iris trait to a 9 kb region and a facilitative glucose transporter gene SLC2A11B. A nonsense mutation W49X leading to a premature stop codon in SLC2A11B was identified as the causal variant. Transcriptome analysis suggested that SLC2A11B loss-of-function may downregulate the xanthophore-differentiation gene CSF1R, and a key gene GCH1 involved in biosynthesis of pteridine, whose absence results in pearl iris. Coalescence and phylogenetic analyses indicated the mutation originated about 5,400 years ago coinciding with the onset of pigeon domestication, while positive selection was detected likely associated with artificial breeding. Within Aves, potentially impaired SLC2A11B was found in 10 species from six distinct lineages correlated to their signature brown or blue eyes. Analysis of vertebrate SLC2A11B orthologs revealed relaxed selection in the avian clade, consistent with the scenario that, during and after avian divergence from reptile ancestor, the SLC2A11B-involved development of dermal chromatophores likely degenerated due to feather coverage. Our findings provide new insight into the mechanism of avian iris color variations and the evolution of pigmentation in vertebrates.

SUMMARYHagfish eyes are markedly basic compared to the eyes of other vertebrates, lacking a pigmented epithelium, a lens, and a retinal architecture built of three cell layers – the photoreceptors, interneurons & ganglion cells. Concomitant with hagfish belonging to the earliest-branching vertebrate group (the jawless Agnathans), this lack of derived characters has prompted competing interpretations that hagfish eyes represent either a transitional form in the early evolution of vertebrate vision, or a regression from a previously elaborate organ. Here we show the hagfish retina is not extensively degenerating during its ontogeny, but instead grows throughout life via a recognizable Pax6+ ciliary marginal zone. The retina has a distinct layer of photoreceptor cells that appear to homogeneously express a single opsin of the rh1 rod opsin class. The epithelium that encompasses these photoreceptors is striking because it lacks the melanin pigment that is universally associated with animal vision; notwithstanding, we suggest this epithelium is a homolog of gnathosome Retinal Pigment Epithelium (RPE) based on its robust expression of RPE65 and its engulfment of photoreceptor outer segments. We infer that the hagfish retina is not entirely rudimentary in its wiring, despite lacking a morphologically distinct layer of interneurons: multiple populations of cells exist in the hagfish inner retina that differentially express markers of vertebrate retinal interneurons. Overall, these data clarify Agnathan retinal homologies, reveal characters that now appear to be ubiquitous across the eyes of vertebrates, and refine interpretations of early vertebrate visual system evolution.HIGHLIGHTSHagfish eyes are degenerate but not degenerating, i.e. rudimentary but growingRetinal interneurons discovered implying ancestral hagfish had derived retinas & visionDespite lacking pigment, a Retinal Pigmented Epithelium homolog functions in hagfishRevised synapomorphies illuminate the dimly lit origins of vertebrate eye evolutionGRAPHICAL ABSTRACT

The evolution of the vertebrate eye remains so far unresolved. Amphioxus frontal eye pigment cells and photoreceptors were proposed to be homologous to vertebrate photoreceptors and retinal pigmented epithelium, based on ultrastructural morphology and gene expression analysis in B. floridae. Here, we present comparative molecular data using two additional amphioxus species, a closely related B. lanceolatum, and the most divergent A. lucayanum. Taking advantage of a unique set of specific antibodies we characterized photoreceptors and putative interneurons of the frontal eye and investigated its neuronal circuitry. Our results corroborate generally conserved molecular fingerprint among cephalochordate species. Furthermore, we performed pharmacological perturbations and found that the Notch signaling pathway, a key regulator of retina development in vertebrates, is required for correct ratios among frontal eye cell types. In summary, our study provides a valuable insight into cell-type relationships in chordate visual organs and strengthens the previously proposed homology between amphioxus frontal eye and vertebrate eyes.

Revealing the mechanisms underlying the breath-taking morphological diversity observed in nature is a major challenge in Biology. It has been established that recurrent mutations in hotspot genes cause the repeated evolution of rather simple morphological traits, such as body pigmentation or the gain and loss of structures. To date, however, it remains elusive whether hotspot genes contribute to natural variation in complex morphological traits, such as the size and shape of organs. Since natural variation in head morphology is pervasive inDrosophila, we studied the molecular and developmental basis of differences in compound eye size and head shape in two closely relatedDrosophilaspecies. We show that differences in both traits are established late during head development and we applied comparative transcriptomics and chromatin accessibility data to identify the GATA transcription factor Pannier (Pnr) as central factor regulating these differences. Although the genetic manipulation of Pnr affected multiple aspects of dorsal head development, the effect of natural variation is restricted to a subset of the phenotypic space. We present data suggesting that this developmental constraint is caused by the co-evolution of expression ofpnrand its co-factoru-shaped (ush). We propose that natural variation in highly connected developmental regulators with pleiotropic functions is a major driver for morphological evolution and we discuss implications on gene regulatory network evolution. In comparison to previous findings, our data strongly suggests that evolutionary hotspots do not contribute to the repeated evolution of eye size and head shape inDrosophila.

Photoreceptor cells in the eyes of Bilateria are often classified into microvillar cells with rhabdomeric opsin and ciliary cells with ciliary opsin, each type having specialized molecular components and physiology. First data on the recently discovered xenopsin point towards a more complex situation in protostomes. In this study, we provide clear evidence that xenopsin enters cilia in the eye of the larval bryozoanTricellaria inopinataand triggers phototaxis. As reported from a mollusc, we find xenopsin coexpressed with rhabdomeric-opsin in eye photoreceptor cells bearing both microvilli and cilia in larva of the annelidMalacoceros fuliginosus. This is the first organism known to have both xenopsin and ciliary opsin, showing that these opsins are not necessarily mutually exclusive. Compiling existing data, we propose that xenopsin may play an important role in many protostome eyes and provides new insights into the function, evolution, and possible plasticity of animal eye photoreceptor cells.

The fine structure of the larval eyes of the hangingfly Terrobittacus implicatus (Huang & Hua) was investigated using scanning and transmission electron microscopy. The results show that the larval eyes of T. implicatus each consist of seven spaced ommatidia. Each ommatidium is composed of a corneal lens with about 45 lamellae, a tetrapartite eucone type of crystalline cone, eight retinula cells, two primary pigment cells, and an undetermined number of secondary pigment cells. The rhabdomeres of eight retinula cells effectively fuse into a centrally-fused, tiered funnel-shaped rhabdom extending from the base of the crystalline cone deeply into the ommatidium. In light of different positions in the ommatidium, the retinula cells can be divided into four distal and four proximal retinula cells. Pigment cells envelop the entire ommatidium. Electron-lucent vesicles are abundant throughout the cytoplasm of the eight retinula cells. The larval ommatidia of T. implicatus are similar to those of the Panorpidae, except for the distal retinula cells that also participate in the formation of the proximal rhabdom. In this case, the larval eyes of T. implicatus may lie in the transitional stage during the larval eye evolution of insects from ommatidia to stemmata.

Only a few studies have examined the visual system of Pseudoscorpiones until now. To fill this knowledge gap we analysed the axonal trajectories and neuropil architecture of the visual system of the pseudoscorpion Neobisium carcinoides (Hermann, 1804) with different neuroanatomical techniques. The R-cell axon terminals were identified with Cobalt fills and the morphology of the visual neuropils and the protocerebrum generally is described by means of the osmium-ethyl gallate procedure and TEM. N. carcinoides has two lateral eyes on each side of the prosoma. The R-cells of the eyes per hemisphere are linked to a first and a second visual neuropil, located in the dorsolateral protocerebrum. The first visual neuropil is subdivided into two hemineuropils, one for each lateral eye, while the second neuropil is not. Furthermore, the two-layered arcuate body is found − isolated from the visual neuropils − in the midline of the protocerebrum at a dorsoposterior position. These findings allow a detailed comparison of the pseudoscorpion visual system with that of other previously studied taxa and shed new light on lateral eye evolution in Chelicerata.

Simple roles for photoreception are likely to have preceded more demanding ones such as vision. The driving force behind this evolution is the improvement and elaboration of animal behaviors using photoreceptor input. Because the basic role for all senses aimed at the external world is to guide behavior, we argue here that understanding this "behavioral drive" is essential for unraveling the evolutionary past of the senses. Photoreception serves many different types of behavior, from simple shadow responses to visual communication. Based on minimum performance requirements for different types of tasks, photoreceptors have been argued to have evolved from non-directional receptors, via directional receptors, to low-resolution vision, and finally to high-resolution vision. Through this sequence, the performance requirements on the photoreceptors have gradually changed from broad to narrow angular sensitivity, from slow to fast response, and from low to high contrast sensitivity during the evolution from simple to more advanced and demanding behaviors. New behaviors would only evolve if their sensory performance requirements to some degree overlap with the requirements of already existing behaviors. This need for sensory "performance continuity" must have determined the order by which behaviors have evolved and thus been an important factor guiding animal evolution. Naturally, new behaviors are most likely to evolve from already existing behaviors with similar neural processing needs and similar motor responses, pointing to "neural continuity" as another guiding factor in sensory evolution. Here we use these principles to derive an evolutionary tree for behaviors driven by photoreceptor input.

Vertebrates exhibit substantial variation in eye size. Eye size correlates positively with visual capacity and behaviors that enhance fitness, such as predator avoidance. This foreshadows a connection between predation and eye size evolution. Yet, the conditions that favor evolutionary shifts in eye size, besides the well-known role for light availability, are unclear. We tested the influence of predation on the evolution of eye size in Trinidadian killifish, Rivulus hartii. Rivulus are located across a series of communities where they coexist with visually oriented piscivores ("high predation" sites), and no predators ("Rivulus-only" sites). Wild-caught Rivulus from high predation sites generally exhibited a smaller relative eye size than communities that lack predators. Yet, such differences were inconsistent across rivers. Second-generation common garden reared fish revealed repeatable decreases in eye size in Rivulus from high predation sites. We performed additional experiments that tested the importance of light and resources on eye size evolution. Sites that differ in light or resource availability did not differ in eye size. Our results argue that differences in predator-induced mortality underlie genetically-based shifts in vertebrate eye size. We discuss the drivers of eye size evolution in light of the nonparallel trends between the phenotypic and common garden results.

Eye regression occurs across cave-dwelling populations of many species and is often coupled with a decrease or loss in eye function. Teleost fishes are among the few vertebrates to undergo widespread colonization of caves and often exhibit eye regression with blindness. Cave populations of the poeciliid fish Poecilia mexicana (cave molly) exhibit reduced—albeit functional—eyes, offering the opportunity to investigate partial eye regression. We sequenced eye transcriptomes of cave and surface populations of P. mexicana to identify differentially expressed genes that potentially underlie eye regression in cave mollies. We identified 28 significantly differentially expressed genes, 20 of which were directly related to light sensitivity, eye structure and visual signaling. Twenty-six of these genes were downregulated in cave compared to surface populations. Functional enrichment analysis revealed eye-related gene ontologies that were under-represented in cave mollies. In addition, a set of co-expressed genes related to vision and circadian rhythm was correlated with habitat type (cave versus surface). Our study suggests that differential gene expression plays a key role in the beginning evolutionary stages of eye regression in P. mexicana , shedding further light on regressive evolution in cavefish.

Eyes are quintessential complex traits and our understanding of their evolution guides models of trait evolution in general. A long-standing account of eye evolution argues natural selection favors morphological variations that allow increased functionality for sensing light (Darwin 1859; v. Salvini-Plawen and Mayr 1977; Nilsson and Pelger 1994; Nilsson 2013). While certainly true in part, this focus on visual performance does not entirely explain why diffuse photosensitivity persists even after eyes evolve, or why eyes evolved many times, each time using similar building blocks. Here we briefly review a vast literature indicating most genetic components of eyes historically responded to stress caused directly by light, including UV damage of DNA, oxidative stress, and production of aldehydes. We propose light-induced stress had a direct and prominent role in the evolution of eyes by bringing together genes to repair and prevent damage from light-stress, both before and during the evolution of eyes themselves. Stress-repair and stress-prevention genes were perhaps originally deployed as plastic responses to light and/or as beneficial mutations genetically driving expression where light was prominent. These stress-response genes sense, shield, and refract light but only as reactions to ongoing light stress. Once under regulatory-genetic control, they could be expressed before light stress appeared, evolve as a module, and be influenced by natural selection to increase functionality for sensing light, ultimately leading to complex eyes and behaviors. Recognizing the potentially prominent role of stress in eye evolution invites discussions of plasticity and assimilation and provides a hypothesis for why similar genes are repeatedly used in convergent eyes. Broadening the drivers of eye evolution encourages consideration of multi-faceted mechanisms of plasticity/assimilation and mutation/selection for complex novelties and innovations in general.

The fruit fly Drosophila melanogaster has two types of external visual organs, a pair of compound eyes and a group of three ocelli. At the time of neurogenesis, the proneural transcription factor Atonal mediates the transition from progenitor cells to differentiating photoreceptor neurons in both organs. In the developing compound eye, atonal (ato) expression is directly induced by transcriptional regulators that confer retinal identity, the Retinal Determination (RD) factors. Little is known, however, about control of ato transcription in the ocelli. Here we show that a 2kb genomic DNA fragment contains distinct and common regulatory elements necessary for ato induction in compound eyes and ocelli. The three binding sites that mediate direct regulation by the RD factors Sine oculis and Eyeless in the compound eye are also required in the ocelli. However, in the latter, these sites mediate control by Sine oculis and the other Pax6 factor of Drosophila, Twin of eyeless, which can bind the Pax6 sites in vitro. Moreover, the three sites are differentially utilized in the ocelli: all three are similarly essential for atonal induction in the posterior ocelli, but show considerable redundancy in the anterior ocellus. Strikingly, this difference parallels the distinct control of ato transcription in the posterior and anterior progenitors of the developing compound eyes. From a comparative perspective, our findings suggest that the ocelli of arthropods may have originated through spatial partitioning from the dorsal edge of an ancestral compound eye.

Summary The distribution of lateral eyes in arachnids and their relatives (Chelicerata) is reviewed, including novel data for selected taxa. Particular focus was given to camel spiders (Solifugae) and whip scorpions (Thelyphonida), for which there are conflicting reports about their eye morphology in the literature, and to the condition in some fossil scorpions (Scorpiones) and some extinct trigonotarbid arachnids (Trigonotarbida), which have lateral eyes with c. 30 or up to 15 individual lenses, respectively. Arachnid outgroups like horseshoe crabs (Xiphosura) and sea scorpions (Eurypterida) have compound lateral eyes, but the hypothesis that reduction of these eyes to five lenses or fewer is a synapomorphy of Arachnida can be rejected. Fossil data indicate, instead, that the arachnid lateral eyes were also originally (semi-) compound, and that reduction to only a handful of lenses must be a homoplastic character state. Note that camel spiders retain vestigial lateral eyes, while fossil ricinuleids had a...

The cephalopod visual system is an exquisite example of convergence in biological complexity. However, we have little understanding of the genetic and molecular mechanisms underpinning its elaboration. The generation of new genetic material is considered a significant contributor to the evolution of biological novelty. We sought to understand if this mechanism may be contributing to cephalopod-specific visual system novelties. Specifically, we identified duplications in the Krüppel-like factor/specificity protein (KLF/SP) sub-family of C2H2 zinc-finger transcription factors in the squid Doryteuthis pealeii . We cloned and analysed gene expression of the KLF/SP family, including two paralogs of the DpSP6-9 gene. These duplicates showed overlapping expression domains but one paralog showed unique expression in the developing squid lens, suggesting a neofunctionalization of DpSP6-9a . To better understand this neofunctionalization, we performed a thorough phylogenetic analysis of SP6-9 orthologues in the Spiralia. We find multiple duplications and losses of the SP6-9 gene throughout spiralian lineages and at least one cephalopod-specific duplication. This work supports the hypothesis that gene duplication and neofunctionalization contribute to novel traits like the cephalopod image-forming eye and to the diversity found within Spiralia.

The evolution of eye loss in subterranean, deep sea, and nocturnal habitats has fascinated biologists since Darwin wrestled with it in On the Origin of Species. This phenomenon appears consistently throughout the animal kingdom, in groups as diverse as crustaceans, salamanders, gastropods, spiders, and the well-known Mexican cave fish, but the nature, extent, and evolutionary processes behind eye loss remain elusive. With the advantage of new imaging, molecular, and developmental tools, eye loss has once again become the subject of intense research focus. To advance our understanding of eye loss as a taxonomically widespread and repeated evolutionary trajectory, we organized a cross-disciplinary group of researchers working on the historic question, "how does eye loss evolve in the dark?." The resulting set of papers showcase new progress made in understanding eye loss from the diverse fields of molecular biology, phylogenetics, development, comparative anatomy, paleontology, ecology, and behavior in a wide range of study organisms and habitats. Through the integration of these approaches, methods, and results, common themes begin to emerge across the field. For the first time, we hope researchers can exploit this new synthesis to identify the broader challenges and key evolutionary questions surrounding eye evolution and so-called regressive evolution and collectively work to address them in future research.

It has been speculated that the unitary eyes of vertebrates and molluscs, and the compound eyes of insects and crustaceans, evolved separately. On the other hand, the common use of rhodopsin as a photoreceptor molecule, and the conservation of Pax6 as a master control gene for eye development, suggest instead that the eye evolved once. Yet, recently the molecular genetics that had seemed to suggest a definitive answer to this evolutionary point has once again become cloudy. Here we propose an alternative approach to addressing the question of eye evolution through comparative analyses of physiological optics. Serendipitous discoveries involving form deprivation and defocusing with young monkeys and chicks demonstrated the conserved importance of visual experience on eye development. Similar results have been demonstrated in teleosts, although differences exist in eye anatomy, physiology and optics. In particular, since fish grow throughout life, these effects can also be demonstrated in adults. In comparison, the cephalopod eye is an often-cited example of convergent evolution with the vertebrate eye, although considerable developmental differences exist. Nevertheless, squid eyes from animals raised under alternative lighting exhibit anatomical and refractive changes that agree with those found in vertebrates. Together, these observations provide functional and structural support for the view that the eye evolved once. Because of their very compressed lifespans (only one to two years) cephalopods may be ideal animal models for the study of ocular refractive development.

Geckos feature a large range of eye sizes, but what drives this phenotypic diversity is currently unknown. Earlier studies point towards diel activity patterns (DAPs) and locomotory mode, but phylogenetic comparative studies in support of the proposed adaptive mode of eye evolution are lacking. Here, we test the hypothesis of DAPs as the driver of eye size evolution with a dataset on 99 species of gecko. Results from phylogenetic generalized least-square analysis (PGLS) and multivariate model-fitting reveal smaller eyes in diurnal geckos consistent with different phenotypic optima. However, Bayesian analyses of selective regime shifts demonstrate that only two of nine transitions from nocturnal to diurnal activity are coupled with decreases in eye size, and two other regime shifts are not associated with DAP transitions. This non-uniform evolutionary response suggests that eye size is not the only functionally relevant variable. Evolutionary adaptations may therefore include different combinations of several traits (e.g. photoreceptors), all with the same functional outcome. Our results further demonstrate that DAP only partially explains eye size diversity in geckos. As open habitats favour the evolution of large eyes while obstructed habitats favour small eyes, the degree of habitat clutter emerges as another potential axis of eye diversification.

To better understand relationships between the structures and functions of the distributed visual systems of chitons, we are comparing how morphological differences between the light-sensing structures of these animals relate to their visually-guided behaviors. All chitons have sensory organs – termed aesthetes – embedded within their protective shell plates. In some species, the aesthetes are interspersed with small, image-forming eyes. In other species, the aesthetes are paired with pigmented eyespots. Previously, we compared the visually-influenced behaviors of chitons with aesthetes to those of chitons with both aesthetes and eyes. Here, we characterize the visually-influenced behaviors of chitons with aesthetes and eyespots. We find that chitons with eyespots engage in behaviors consistent with spatial vision, but appear to use spatial vision for different tasks than chitons with eyes. Unlike chitons with eyes, Chiton tuberculatus and C. marmoratus fail to distinguish between sudden appearances of overhead objects and equivalent, uniform changes in light levels. We also find that C. tuberculatus orients to static objects with angular sizes as small as 10°. Thus, C. tuberculatus demonstrates spatial resolution that is at least as fine as that demonstrated by chitons with eyes. The eyespots of Chiton are smaller and more numerous than the eyes found in other chitons and they are separated by angles of

Fan worms, represented by sabellid and serpulid polychaetes, have an astonishing array of unusual eyes and photoreceptors located on their eponymous feeding appendages. Here we organize the previous descriptions of these eyes in serpulids and report new anatomical, molecular, and physiological data regarding their structure, function, and evolution and the likely identity of their phototransduction machinery. We report that, as in sabellids, serpulids display a broad diversity of radiolar eye arrangements and ocellar structures. Furthermore, the visual pigment expressed in the eyes of Spirobranchus corniculatus, a species of the charismatic Christmas tree worms, absorbs light maximally at 464 nm in wavelength. This visual pigment closely matches the spectrum of downwelling irradiance in shallow coral reef habitats and lends support to the hypothesis that these radiolar photoreceptors function as a silhouette-detecting "burglar alarm" that triggers a rapid withdrawal response when the worm is threatened by potential predators. Finally, we report on the transcriptomic sequencing results for the radiolar eyes of S. corniculatus, which express invertebrate c-type opsins in their ciliary radiolar photoreceptors, closely related to the opsin found in the radiolar eyes of the sabellid Acromegalomma interruptum. We explore the potential for a shared evolutionary lineage between the radiolar photoreceptors of serpulids and sabellids and consider these unique innovations in the broader context of metazoan eye evolution.

International audience; In metazoans, there is a remarkable diversity of photosensitive structures; their shapes, physiology, optical properties, and development are different. To approach the evolution of photosensitive structures and visual function, cephalopods are particularly interesting organisms due to their most highly centralized nervous system and their camerular eyes which constitute a convergence with those of vertebrates. The eye morphogenesis in numerous metazoans is controlled mainly by a conserved Retinal Determination Gene Network (RDGN) including pax, six, eya, and dac playing also key developmental roles in non-retinal structures and tissues of vertebrates and Drosophila. Here we have identified and explored the role of Sof-dac, Sof-six1/2, Sof-eya in eye morphogenesis, and nervous structures controlling the visual function in Sepia officinalis. We compare that with the already shown expressions in eye development of Sof-otx and Sof-pax genes. Rhodopsin is the pigment responsible for light sensitivity in metazoan, which correlate to correlate visual function and eye development. We studied Sof-rhodopsin expression during retina differentiation. By in situ hybridization, we show that (1) all of the RDGN genes, including Sof-pax6, are expressed in the eye area during the early developmental stages but they are not expressed in the retina, unlike Sof-otx, which could have a role in retina differentiation; (2) Sof-rhodopsin is expressed in the retina just before vision gets functional, from stage 23 to hatching. Our results evidence a role of Sof-six1/2, Sof-eya, and Sof-dac in eye development. However, the gene network involved in the retinal photoreceptor differentiation remains to be determined. Moreover, for the first time, Sof-rhodopsin expression is shown in the embryonic retina of cuttlefish suggesting the evolutionary conservation of the role of rhodopsin in visual phototransduction within metazoans. These findings are correlated with the physiological and behavioral observations suggesting that S. officinalis is able to react to light stimuli from stage 25 of organogenesis on, as soon as the first retinal pigments appear.

Bilateral symmetry is assumed to contribute to the evolution of eye color, with the left and right eye being the same color in most vertebrates; yet, few studies tested this assumption. Here, we compared the amount of iris flecking (black spots presented on the iris) between the left and right eye of 76 adult common cuckoos Cuculus canorus. We found considerable variation in the total amount of iris flecking among individuals, with variation being associated with body size and sex. We also found that the amount of iris flecking differed between the left and right eye and that this left-right asymmetry was not random, with the left eye almost always being darker than the right eye. Furthermore, this asymmetry was negatively associated with wing length; however, this effect was limited to individuals with dark eyes. Overall, the asymmetric, but non-random, distribution of iris flecking between the left and right eye may indicate that selection pressures driving asymmetry (such as visual lateralization) act on the development of iris colors, even though this effect might be limited, due to the role of bilateral symmetry.

In comparison to complex visual systems, non-directional photoreception – the most primitive form of biological photodetection – has been poorly investigated, although it is essential to many biological processes such as circadian and seasonal rhythms. Here we describe the spatiotemporal expression pattern of the major molecular actors mediating light reception – opsins – localized in the Strongylocentrotus purpuratus larva. In contrast to other zooplanktonic larvae, the echinopluteus lacks photoreceptor cells with observable shading pigments involved in directional visual tasks. Nonetheless, the echinopluteus expresses two distinct classes of opsins: a Go-opsin and a rhabdomeric opsin. The Go-opsin, Sp-opsin3.2, is detectable at early (3 days post fertilization) and four armed pluteus stages (4 days post fertilization) in two cells that flank the apical organ. To rule out the presence of shading pigments involved in directional photoreception, we used electron microscopy to explore the expression domain of Go-opsin Sp-opsin3.2 positive cells. The rhabdomeric opsin Sp-Opsin4 expression is detectable in clusters of cells located around the primary podia at the five-fold ectoderm pentagonal disc stage (day 18-21) and thereafter, thus indicating that Sp-Opsin4 may not be involved in the photoreception mechanism of the larva, but only of the juvenile. We discuss the putative function of the relevant cells in their neural context, and propose a model for understanding simple photodetection in marine larvae.

Drosophila has three types of visual organs, the larval eyes or Bolwig's organs (BO), the ocelli (OC) and the compound eyes (CE). In all, the bHLH protein Atonal (Ato) functions as the proneural factor for photoreceptors and effects the transition from progenitor cells to differentiating neurons. In this work, we investigate the regulation of ato expression in the BO primordium (BOP). Surprisingly, we find that ato transcription in the BOP is entirely independent of the shared regulatory DNA for the developing CE and OC. The core enhancer for BOP expression, ato BO , lies ~6 kb upstream of the ato gene, in contrast to the downstream location of CE and OC regulatory elements. Moreover, maintenance of ato expression in the neuronal precursors through autoregulation—a common and ancient feature of ato expression that is well-documented in eyes, ocelli and chordotonal organs—does not occur in the BO. We also show that the ato BO enhancer contains two binding sites for the transcription factor Sine oculis (So), a core component of the progenitor specification network in all three visual organs. These binding sites function in vivo and are specifically bound by So in vitro . Taken together, our findings reveal that the control of ato transcription in the evolutionarily derived BO has diverged considerably from ato regulation in the more ancestral compound eyes and ocelli, to the extent of acquiring what appears to be a distinct and evolutionarily novel cis -regulatory module.

The opsin gene family encodes key proteins animals use to sense light and has expanded dramatically since it originated early in animal evolution. Understanding the origins of opsin diversity can offer clues to how separate lineages of animals have repurposed different opsin paralogs for different light-detecting functions. However, the more we look for opsins outside of eyes and from additional animal phyla, the more opsins we uncover, suggesting we still do not know the true extent of opsin diversity, nor the ancestry of opsin diversity in animals. To estimate the number of opsin paralogs present in both the last common ancestor of the Nephrozoa (bilaterians excluding Xenoacoelomorpha), and the ancestor of Cnidaria + Bilateria, we reconstructed a reconciled opsin phylogeny using sequences from 14 animal phyla, especially the traditionally poorly-sampled echinoderms and molluscs. Our analysis strongly supports a repertoire of at least nine opsin paralogs in the bilaterian ancestor and at least four opsin paralogs in the last common ancestor of Cnidaria + Bilateria. Thus, the kernels of extant opsin diversity arose much earlier in animal history than previously known. Further, opsins likely duplicated and were lost many times, with different lineages of animals maintaining different repertoires of opsin paralogs. This phylogenetic information can inform hypotheses about the functions of different opsin paralogs and be used to understand how and when opsins were incorporated into complex traits like eyes and extraocular sensors.

How transcriptional gene networks operate during development and how they have emerged during evolution are two fundamental and interconnected questions in the evo-devo field (Davidson in The regulatory genome: gene regulatory networks in development and evolution. Academic Press, Amsterdam, 2006; Carroll in Cell 134(1):25–36, 2008). In this chapter we discuss the origin of the vertebrate eye from a common ancestor and its gene regulatory network (GRN). In an attempt to shed light on the evolutionary history of the vertebrate eye, photoreceptive structures present in our chordate sister groups cephalochordates (lancelets) and urochordates (tunicates) will be examined. Additionally, we summarize the still fragmentary information on the specification of visual organs in these chordate groups., This work was supported by grants BFU2011-22916, BFU2014-53765-P, and P11-CVI-7256 to JRMM.

Developmental genetics of Drosophila continue to have a great impact on our understanding of evolution. The specification of the body plan involves four conceptual steps: 1) Localization of maternal mRNAs in the egg cytoplasm. 2) Translation of these RNAs and formation of morphogen gradients. 3) Subdivision of the antero-posterior gradient into a repetitive pattern of body segments. 4) Assignment of a specific identity to each segment by the Hox genes. The discovery of the Hox genes has uncovered a universal principle shared by all bilaterians; they serve as master control genes specifying organization along the antero-posterior axis. The ancestral arthropods presumably consisted of a series of more or less identical segments, which may be represented by recently discovered precambrian Lobopodia which have a pair of legs and a pair of eyes in each segment. The progressive divergence of Hox genes has led to progressive cephalization and caudalization. From the amino acid sequences of the clustered homeodomains we can deduce that the mesothoracic segment represents the prototype from the more anterior and the more posterior segments evolved. Pax6 has been identified as a master control gene for eye development in all bilaterians. Since Pax6 is involved in eye development in all bilaterian phyla, this argues strongly for a monophyletic origin of the metazoan eye. With the same tool box of transcription factors all the different eye-types can be constructed.

A retractable head region somewhat resembling the introvert of sipunculans is a characteristic feature of members of the annelid taxon Fauveliopsidae. The morphology of fauvelopsids is not well known, and additional data might help to resolve their relationships with other annelids and sipunculans. Ultrastructural investigations of the anterior end of adults of Fauveliopsis cf. adriatica revealed peculiar brain and sensory structures. From the neuropil of the brain, two pairs of lobes mainly composed of neuronal somata extend posteriorly into the peristomium and the following segment. The nuchal organs are embedded in the median pair of lobes, as are additional photoreceptor-like sensory structures, the ocellar tubes, which are found at the bases of epidermal follicles that extend deeply into the brain. The retractor muscles of the prostomium are attached to the apices of these follicles, which are lined by tendon and supportive cells. The lumen of each follicle is completely filled with cuticular material that forms a rod. Monociliary sensory cells are present all along the length of each follicle; their cilia extend into the cuticle, and are oriented parallel to the longitudinal axis of the tube. Basally, each follicle forms an ovoid extension that is devoid of cuticular material and densely filled with numerous sensory processes—microvilli and cilia—of bipolar sensory cells. The terminal end of the 40-μm-deep follicle is formed by two conspicuous cells that contain numerous densely packed vesicles that resemble pigment granules. The ocellar tubes of fauveliopsids are strikingly similar to the ocular tubes of sipunculids. These similarities may reflect common ancestry or may represent convergent evolution; both alternatives are partially supported by previous morphological and molecular studies.

The fossil record of arthropod compound eyes reflects different modes and occasions of eye reduction and blindness. In the best-studied fossil examples, the trilobites [trilobites: extinct arthropods, dominant during the Palaeozoic], which have an excellent geological record, eyes are primary structures, and in all known genera which lack them, eye-loss is always secondary. Once the eyes were lost, they never were never re-established. The most striking examples occur in the Upper Devonian, when two unrelated major groups of trilobites, with different kinds of eyes, underwent eye reduction and even total loss of the eyes over the same time period, undoubtedly due to long-term environmental change. One reason is that a mud blanket spread over a vast area, there was no firm substrate, and many trilobites became small and many became endobenthic, reducing or losing their eyes in the process. Toxic environmental conditions may also have had an effect. Certain coeval forms remained, however, which still possess perfectly good compound eyes. Either they found vacant refuges where they could survive, or alternatively their visual systems were elaborate enough to adapt to the changing conditions. Another inducement for evolving small, reduced compound eyes is to become a tiny organism oneself, with simply not enough space to establish a regular and functional compound eye, and in such minaturised eyes special adaptations for capturing enough photons are necessary. Thus very small compound eyes often establish wide acceptance angles of their ommatidia, collecting light over large angular ranges of space and it is beneficial to have a wide rhabdom provided that it is short, has a wide lens diameter, and perhaps even possess highly sensitive receptor cells. We find such a miniaturised system in the first recorded planktonic trilobite. Another kind of reduction of a compound eye, or parts of it, also occurs, if selective pressure claims for a high specialisation of eyes that results in several facets fusing into a single functional unit. This probably can be found in phacopid trilobites, ~400 million years old. Here the enlarged aperture of a resulting large lens may allow vision under dim light conditions such as at greater depth. The fossil record gives relatively little evidence about parasites, which often have reduced eyes. Agnostida are blind relatives of trilobites which lived during the Cambrian and Ordovician. An early suggestion was that some of these were parasitic, but this was never commonly adopted. Finally penstastomids (Crustacea), worm-like parasitic organisms, already have been blind from the Cambrian (~487Ma).

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.

Meeting the challenge of sampling an ancient aquatic landscape by the early vertebrates was crucial to their survival and would establish a retinalbauplanto 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.

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.

The general expression of the transcription factor gene Pax-6 homologues and the overall presence of the photopigment opsin have cast doubt on the polyphyletic evolution of photoreceptors. Herein it is proposed that the evolutionary pathway of photoreceptors reflects two different, successive processes: (i) the (monophyletic?) differentiation of photoreception as such, mediated by a specific transcription factor gene (such as Pax-6 or sine oculis) and (ii) the genetic information of that induction factor (normative unit for photoreception). The latter stimulates the (polyphyletic) differentiation of the photoreceptors themselves through its multiply convergent co-options with variable network-modifications (intercalation of different genes). The expression of transcription factor genes does not per se imply homology of the differentiated photoreceptors (but at most some pattern of homoiology). The differentiation of both receptor types, ciliary versus rhabdomeric, in one and the same cell during...

Animal eyes generally fall into two categories: (1) their photoreceptive array is convex, as is typical for camera eyes, including the human eye, or (2) their photoreceptive array is concave, as is typical for the compound eye of insects. There are a few rare examples of the latter eye type having secondarily evolved into the former one. When viewed in a phylogenetic framework, the head morphology of a variety of male scale insects suggests that this group could be one such example. In the Margarodidae (Hemiptera, Coccoidea), males have been described as having compound eyes, while males of some more derived groups only have two single-chamber eyes on each side of the head. Those eyes are situated in the place occupied by the compound eye of other insects. Since male scale insects tend to be rare, little is known about how their visual systems are organized, and what anatomical traits are associated with this evolutionary transition. In adult male Margarodidae, one single-chamber eye (stemmateran ocellus) is present in addition to a compound eye-like region. Our histological investigation reveals that the stemmateran ocellus has an extended retina which is formed by concrete clusters of receptor cells that connect to its own first-order neuropil. In addition, we find that the ommatidia of the compound eyes also share several anatomical characteristics with simple camera eyes. These include shallow units with extended retinas, each of which is connected by its own small nerve to the lamina. These anatomical changes suggest that the margarodid compound eye represents a transitional form to the giant unicornal eyes that have been described in more derived species.