Abstract
A majesty of evolution encompasses in diversity of the types of eyes known today. Out of all organisms, only a bit over 30 different phyla possess sophisticated eyes. Stating that, rest of the animals are not blind. There could be camera type, or compound eyes, or mirror-like eyes, all different from one another in several aspects, still performing more or less the same function. Even though there are several differences, there are striking similarities as well in all diverse animal life forms. After Ramon y Cajal observed striking similarities between vertebrate and insect retinas, over a century ago, newer research keeps adding to the account with the help of cutting edge technology. Today, we know for the fact that there are more similarities than one can think into visual systems of insects and vertebrates. Of all invertebrate model systems, Drosophila melanogaster stands apart; for, it shares a high degree of genetic conservation and less redundancy. Shorter life span, ease of culture, and availability of wide variety of genetic tools are other benefits which make Drosophila melanogaster a great model system. In this chapter, we shall be providing a comparative account on the compound eye of Drosophila melanogaster with that of camera type eye of vertebrates, in terms of development, structure, and physiology.
Access provided by Autonomous University of Puebla. Download chapter PDF
Similar content being viewed by others
Keywords
- Drosophila eye
- Compound eye
- Camera type eye
- Ommatidia
- Evolution
- Genetic basis of retinal differentiation and development
Introduction
Eyes, as mentioned by philosopher William Paley, are “miracle of design.” Eyes are indeed amazing organs in the animal kingdom, for their ability to provide a unique sense that makes most of the animals stand apart from rest of the living organisms. Although not all kingdoms of life are devoid of visual senses, the ability to connect sense of vision to that of complex nervous system for processing and image formation is unique to the animal kingdom. Diversity of the eyes in the animal kingdom has been attributed to evolution over a large period of time. Based on evidences from fossil records, first eyes appear some 540 million years ago (Parker 2009). There are different kinds of eyes animals possess, which work in different fashions, in order to “sense” the objects, and may be to form an image. Of all diverse life forms, eye of Drosophila melanogaster is an example of eyes; for an eye; for, it has compound eyes, for sensing, processing and forming the image. For over a century now, Drosophila melanogaster eye has provided a new dimension to several different aspects of understanding in the fields of development and several different diseases (Borst 2009). Santiago Ramon y Cajal, a neuroanatomist was the first to notice the similarities between the visual system of vertebrates and that of the insects. He documented a striking similarity between the neuronal circuits that form the major framework of visual system in flies and vertebrates (Cajal and Sanchez 1915). Compound eyes are built as convex structures around the outside of an animal’s head, and even though their arrangement looks similar to vertebrate eyes (both sides of head), they are fundamentally different from the concave structure of single chamber eyes (Fig. 1). In spite of this major topological difference, however, the jobs of the two kinds of structure are the same: to utilize the incoming light and to develop a sense of vision (Pak 2010; Sanes and Zipursky 2010). For eye is of interest to many research fields, in order to stay focused, we compare the anatomy and function while dwelling into events of genesis of the eye in the embryonic stages, and their genetic regulation.
We shall provide the major similarities and differences in the structure, function, and development of the camera type eyes with those of compound eyes of Drosophila melanogaster in subsequent sections.
Anatomy of Vertebrate Eye
The arrangement of the eye is extremely intricate as indicated (Fig. 1). The entry of light into the eye is facilitated by the cornea. The cornea is thin and transparent. Its transparency arises from an acellular stroma between a layer of epithelial cells and a layer of endothelial cells. It contains no blood vessels to avoid attenuating the light entering the eyes. The cornea receives nourishment from tears on the outside and aqueous humor on its inner surface. The cornea acting in conjugation with the lens focuses light onto the light detecting cells of the eyes—the photoreceptors. The lens too is highly transparent, an adaptation to maximize the light transmitted into the light-sensitive cells of the eye. The lens allows for its shape to be changed in order to allow accommodation of images at different distances and change the focus of the lens. The lens is held in place by the zonular fibers that extend to ciliary body. The contraction of the ciliary muscles facilitates the change of shape of the lens. The forces of ciliary muscles are conveyed to the lens via the zonular fibers. The contraction of the ciliary muscles releases the tension in the zonular fibers and allows the lens to become more round allowing change in the focal plane of the lens-cornea system. Though the cornea achieves most of the focusing function, it has a fixed focus, thus imparting the important function of accommodation to the lens. The lens unlike the cornea is transparent due to the nature of lens cells that constitute it.
The lens fiber cells lose their nuclei and most of their organelles during differentiation. They have high content of proteins called crystallins which do not scatter light like most other proteins. The crystallins have interestingly shown to be expressed in other cells in the body where they have different functional roles such as enzymatic activity (Piatigorsky and Wistow 1989). The iris regulates the entry of light in through the lens. It can dilate or constrict its opening, thus attenuating the light to different extents. The space anterior to the lens is filled with a fluid known as the aqueous humor which is responsible for maintaining the pressure in this compartment of the eye and gives it its shape. The ciliary bodies secrete the aqueous humor. The aqueous humor leaves the eyes through tiny channels in the periphery of the anterior chamber. Posterior to the lens is the vitreous humor which is a denser fluid gel. It exerts a pressure that keeps in place the retina—which is the neuron rich layer responsible for visual computations and relaying the information regarding the visual field to the higher centers in the brain. The retina is followed by the pigmented epithelium and they line the posterior end of the eye. They are followed by the choroid which is rich in vasculature and supplies the outer retinal cells and the photoreceptors together with the pigmented epithelium with nutrients and facilitates gaseous exchange. The output neurons of the retina project to the brain regions via the optic nerve, which is composed of the axons, called the retinal ganglion cells (RGCs) of the retina (the output neurons). The outermost coat of the eye is a tough layer known as the sclera, which is a white tissue. The inner retinal cells receive nourishment and gaseous exchange via the repeated branching of retinal artery.
After portraying the anatomical organization of the eye, it becomes important to understand the retina—the most important part for the early processing of the visual scene and encoding it to be processed by higher brain regions. The retina has a vast diversity in constituent cell types (Fig. 1) that all play a role in the computations performed by the retina that maybe categorized on the basis of molecular identity, morphology, and dendritic stratification patterns (Baden et al. 2016; Gollisch and Meister 2010; Masland 2001, 2012). The subtypes of each cell show a regular arrangement—i.e., there exists a region of exclusion around each cell, where other cells of the same subtype are not found. This leads to a mosaic-like arrangement of each non-reducible neuronal cell subtype—a characteristic feature of the retina. These cells help to convert the image perceived in the visual field into parallel streams of information regarding various features of the image. The neurons of the retina are organized in three cellular layers—the ganglion cell layer, the inner nucleate layer, and the outer nucleate layer. There are two synaptic layers—the inner and outer plexiform layers. These synaptic layers show further stratification. There are six major cell types in the vertebrate retina—the photoreceptors, the horizontal cells, the bipolar cells, the amacrine cells, the ganglion cells, and the glial Muller cells. The photoreceptors—rods and cones—receive photostimulation due to the photopigments (opsins) in these cells responding to impinging photons. The opsin proteins are bound to retinal—a form of Vitamin A. The molecule undergoes isomerization upon absorption of photons, the photosensitive reaction that drives a signaling cascade underlying the function of the retina. The photoreceptors project to the outer nucleate layer where they synapse with the horizontal cells and bipolar cells. The photoreceptors use glutamate as a neurotransmitter. Upon impingement by light, the photoreceptors hyperpolarize—their membrane potential decreases. This leads to a reduced secretion of glutamate which effects the bipolar cells and horizontal cells downstream. The bipolar cells show different functional responses to the light responses of the photoreceptors based on the type of glutamate receptors (both ionic and metabotropic) they express—for example, ON bipolar cells express metabotropic mGluR6 which causes reduced depolarization of the bipolar cell membrane upon binding the glutamate, and hence, when light causes lowered glutamate release from the photoreceptor cells, these cells show increased depolarization of membrane and an ON response to increase in light intensity in their receptive fields. The horizontal cells play a role in feedback and modulate the responses of the photoreceptors. The bipolar cells show wide diversity (Tsukamoto and Omi 2013). The bipolar cells then contact ganglion cells in the inner plexiform layer. Here, a divergence of information occurs and various arrangements of these synaptic contacts and interaction and modulation by the amacrine cells allow for a variety of computations. The ganglion cells have over 30–40 types (Baden et al. 2016) and carry parallel information to the brain about the visual scene. The complex interplay of signals from the bipolar, amacrine, and retinal ganglion cells plays an important role in various features detected and encoded by the retinal ganglion cells. Some instances of these computations include object motion (Baccus et al. 2008), approaching motions (Münch et al. 2009), motion extrapolation amongst other forms of anticipation and adaptations (Chaffiol et al. 2017; Gollisch and Meister 2010; Yao et al. 2018). There are a wide variety of neurotransmitters and receptors involved and they have been implicated in a variety of different functional computations—for instance, dopamine has been implicated in light adaptation of the retina, where the retinal dopamine levels go up with increase in light intensity and seem to be involved in a variety of light adaptive computations that may not be explained by a simple gain control of the retinal cells (Chaffiol et al. 2017; Yao et al. 2018). At the same time, a number of adaptions and functionality of the retina depend on inputs from the brain—retinopetal inputs. This makes it interesting to look at the modulation of signals by various neurotransmitters which are released into the retina by retinopetal neurons in a context-dependent manner. Thus, the mechanism by which the retina computes information cannot be studied independent of these modulating signals.
Anatomy of Drosophila Eye
The major structural components in the retina of Drosophila are the 750 individual units termed as ommatidia which are precisely organized in the lattice (Fig. 1). Each ommatidium consists of eight R cells which are basically the photoreceptor neurons (R1–R8). The photoreceptors can be categorized it is on the basis of opsins they express: R1–R6 type of photoreceptors expresses Rh1 opsins and controls the motion detection, secondly R7 expresses RH3 or Rh4 opsins which are UV-sensitive and lastly R8 expresses either Rh5 (blue) or Rh6 (green) opsins (Salcedo et al. 1999). The photoreceptor cells direct its visual information towards the optic lobe, the primary visual processing center in flies. This optic lobe is composed of four ganglia. First layer is called lamina, beneath it lays the medulla and then the lobula. Mainly in flies, the lobula is further differentiated into lobula and lobula plate (Sinakevitch et al. 2003). The R1–R6 photoreceptors terminate in the first layer lamina while the axons of R7 and R8 end at medulla and hence medulla receives information from the either R7 or R8. In both the R7 and R8 cells, a zinc finger transcription factor called as Sequoia and some N-cadherins are expressed but they majorly control the precise positioning of the axons of photoreceptor R7. Another cell adhesion molecule called Capricious is expressed selectively in R8 cells and regulates the projection of axons of R8 cells (Kulkarni et al. 2016).
The neural circuits are formed of four types of neuronal cells, local neurons or intrinsic neurons, interneurons, photoreceptor axons, and visual projection neurons (VPNs). VPNs connect the optic lobe and the central brain, intrinsic neurons ramify within a single optic ganglion, and interneurons connect more than one ganglion within the optic lobe. Intrinsic neurons, interneurons, and the axons of photoreceptors are oriented in a parallel direction creating a barrel-like structure called the visual cartridge (Otsuna and Ito 2006). The photoreceptor cells collect information from different point and converge it into these parallel columnar synaptic models. The axon of R1–R6 terminates in the lamina and further directs the motion information to the neurons of lamina (L1–L5) in synaptic units. These synaptic units along with amacrine cells and centrifugal interneurons are termed as laminal cartridge (Meinertzhagen and O’neil 1991). The motion information is further transmitted to the underneath ganglia medulla through the axons of lamina neurons L1–L5 each arborized in the particular medulla layers. Along with the axonal projection of the laminal neurons, the axons of R7 and R8 transmit the color information to the M6 and M3 medulla layers, respectively (Takemura et al. 2008; Morante and Desplan 2008). Hence, the parallel columnar organization of the 750 lamina cartridges and medulla column relays the information in a retinotopic fashion that allows the parallel processing of the visual information from different points.
The fly visual system is made up of different neuronal cell types based on the morphology. It can mainly be categorized into two main classes: the uni-columnar neurons and multi-columnar neurons. The uni-columnar neurons are mainly restricted to one column and its projections extend laterally connecting the neighboring columnar modules. The multi-columnar neurons project in several columnar modules. This parallel relay of information either between the layers or columns optimize the signal-to-noise ratio.
Phototransduction and Image Formation
Compound eyes are apposition kind of eyes where optically isolated ommatidia process the images separately. Apposition eyes are typically optimized for high resolution by “apposing” little overlapping visual fields of neighboring ommatidia based on small apertures and rhabdoms (Fig. 2). Each ommatidium receives light; the light is filtered through the lens situated on the outer surface of the eye. Further, the light passes the crystalline cone structure and then through the pigment cells and finally to the visual cells. Each ommatidium ends with its own nerve fiber which connects it to the common optic nerve. Each ommatidia relay its own information and form a tiny image. All the tiny images from each photoreceptor convalesce to form one visual image (Stavenga et al. 2005).
The camera eye of vertebrates produces an inverted image on the light-sensitive elements that is transmitted to the brain via optic nerves (Fig. 2). (Reviewed in Agi et al. 2014).
The phototransduction compartment, the light-guiding rhabdomere is formed by a stack of some 30,000 microvilli, each containing all the essential elements of the transduction cascade. Several elements of these cascades are common elements found in any phosphoinositol cascade, including the G-protein coupled receptor (rhodopsin), heterotrimeric G-protein (Gq), phospholipase C (PLCβ-4), and two closely related Ca2+ channels encoded by the transient receptor potential (trp) and trp-like (trpl) genes.
Development of Eye
The similarities and differences in compound eye of Drosophila versus camera type eye of vertebrates are due to the major differences and similarities of those hailed from embryonic or the developmental stages. Events at different developmental stages are tightly governed by the conserved genetic and molecular mechanisms which are common to both vertebrate and Drosophila eye development.
If it is only about developing an organ, such as an eye, both compound and camera type, what would be required? Assembly of cells, which will eventually differentiate into specialized structures of lens, retina, cornea, photoreceptors, rods, cones, pigment cells, accessory cells, and their neuronal connections to brain. Interestingly, for eye organogenesis, the classical processes of specification, determination, and differentiation follow the same processes for both flies and vertebrates.
Development of eye in both Drosophila and vertebrates begins at early embryonic stages. It is a fascinating process of converting a layer of cells into a three-dimensional functional organ involving axial patterning, followed by proliferation and differentiation. A pioneering research in the field of generation of axes during eye development has indicated that default Drosophila eye primordium is ventral, over which dorsal field is specified as the fly enters and proceeds to larval stages (Singh and Choi 2003; Singh et al. 2006, 2012, 2019). Once the dorsal-ventral axes are specified by specific axial patterning genes, cell proliferation is signaled. Interestingly, these initial events are similar in the development of vertebrate eye as well, described below.
The early stages of vertebrate eye development have been revealed by several embryology experiments, which describe the morphological development of the early eye begins at embryonic day 8.5 (E 8.5), involving formation of an optic vesicle. The optic vesicle contacts head ectoderm to induce thickening of ectoderm forming lens placode. The lens placode invaginates and separates from surrounding ectoderm to form lens vesicle, while optic vesicle folds on itself inward, forming the optic cup. The lens vesicle cells eventually differentiate into lens structures, while optic cup cells form the neural and pigmented layers of the retina (Pei and Rhodin 1970; reviewed in Grainger 1992).
Drosophila eye primordium is ectodermal in origin, which is set aside as a group of only a few number of cells during embryonic stages. Studies have confirmed that the compound eye of Drosophila develops from population of embryonic primordial cells which converge to form anterior head segments, and develop into eye imaginal discs as early as first larval instar stage (Haynie and Bryant 1986; Jürgens et al. 1986; Green et al. 1993; Younossi-Hartenstein et al. 1993; Namba and Minden 1999; Chang et al. 2001; Huang et al. 2017). Imaginal discs are sac-like monolayer epithelial structures which form the blue prints for the adult organs in the Drosophila. The eye imaginal disc is a compound disc, which eventually differentiates into eye, antenna, and the head structures (Fig. 3) (Weismann 1864; Vogt and Anderson 1964; Gehring 1967; Ouweneel 1970; Baker et al. 1978; Haynie and Bryant 1986). During the first and second instar larval stages, eye disc cells divide almost homogeneously and symmetrically by mitosis and imaginal disc grows bigger in size. However, at the end of second instar, or early third instar larval stage, mitotic divisions become asymmetric, for differentiation to begin. A stripe of atonal expression to recognize the R8 cells (Math 5 in vertebrates) determines the apical constriction in posterior cells of the eye disc which appears like a furrow and moves towards the anterior of the eye disc. The stripe of atonal expression defining R8 cells, or the morphogenetic furrow (MF) rather moves like a Mexican wave in the football crowd (described by Jarman 2000). As the MF moves anterior, cells just ahead of it enter G1 arrest and stop proliferating. As cells are released from the furrow, they exit the cell cycle and begin differentiating as the R8, R2/R5/R3/R4 photoreceptor neurons of the pre-cluster. A small subset will undergo a final round of mitosis (the second mitotic wave) before following their sister cells out of the cell cycle and into the ommatidium as the R1/R6/R7 photoreceptors, lens secreting cone cells, and optically insulating pigment cells (Ready et al. 1976; Wolff and Ready 1991; reviewed by Kumar 2018). A fully grown third instar eye disc (Fig. 3) contains antenna, head cuticle blue prints, in addition to differentiated photoreceptor neurons. This monolayer epithelial layer undergoes further changes into pupal stages, which include developing lenses, establishing neuronal connection with the brain, and acquiring pigments to appear a three-dimensional compound eye. After 36 h of pupariation, extra cells between the ommatidia are removed via apoptosis to form the regularly placed hexagonal facets.
It is intriguing that movement of MF in the Drosophila eye disc is required not only for differentiation, but also for regularly spaced photoreceptors; and is indeed similar to movements which occur in some of the vertebrates as well. The Mexican wave-like movement has also been demonstrated during eye development in zebrafish. Neurogenesis begins in optic cup epithelium, closer to optic stalk and then spreads outwards like a wave, which is controlled by atonal homolog ath5.
Genetic Regulation of Eye Development
The highly organized process of eye development is regulated by complex interplay of genetic networks. The advancements in the field of developmental genetics continue to demonstrate a high degree of genetic and molecular conservation during organogenesis of the eye, or oculogenesis between Drosophila and vertebrates. Many of the regulators of eye development were identified in Drosophila by gain-of-function and/or loss-of-function experiments before they were identified and characterized in vertebrate models. Molecular identities began to shine between two systems when Pax6, a member of Paired box family of transcription factor was found to be expressed initially in head ectoderm and optic vesicle, and then became restricted to lens placode ectoderm (Walther and Gruss 1991; Grindley et al. 1995). Despite the distinct morphological differences between the fly and vertebrate eyes, Pax6 homologs, eyeless (ey) (Quiring et al. 1994) and twin of eyeless (toy) (Czerny et al. 1999) provide identity to the eye primordium. Out of two, toy is more similar to Pax6 and acts upstream to ey. Both Pax6 and ey/toy are capable of inducing ectopic eyes in most of the tissues upon overexpression and their mutations result in aniridia in mouse, and no eye phenotypes in flies (Ton et al. 1991; Glaser et al. 1992; Collinson et al. 2000; Quinn et al. 1996; Prosser and van Heyningen 1998; Quiring et al. 1994; Czerny et al. 1999; Halder et al. 1995). Several research labs have demonstrated that both ey and toy are expressed in other non-optic tissues as well, and therefore require other genes to induce the differentiation of the eye. Ectopic induction of ey can induce eye formation in the presence of decapentaplegic (dpp), a TGF-β family of growth factors (Heberlein et al. 1993; Chen et al. 1999). In addition to ey and dpp, other genes which are required for eye development are Eyes absent (Eya) (Bonini et al. 1993), sine oculis (so) (Cheyette et al. 1994), and dachshund (dac) (Mardon et al. 1994). Their vertebrate homologs are EYA 1/EYA2 (Zimmerman et al. 1997), Optix 2/Six 3 (Zuber et al. 1999), and Dach, respectively (Heanue et al. 1999; Ohto et al. 1999). These genes act in concert to aid in eye development (Fig. 4), and their mutations have been shown to cause defects in the eye development/visual impairment. Table 1 summarizes the comparative account on the genes involved in early events for eye development in Drosophila and vertebrates. It is noteworthy that genetic regulation is further accompanied by signaling events which are also conserved in vertebrates and Drosophila. For example, for differentiation of the eye primordium, downstream to ey additional signal from decapentaplegic pathway feeds in to initiate eya and so, which is actually a homolog of Bone Morphogenetic Protein-4/7 (BMP) in vertebrates. However, the difference between flies and vertebrates is, BMPs act in concert with Pax-6 to induce lens placode, which eventually initiates the process of differentiation by inducing Eya and Six-3/Optx-2 (reviewed by Chen et al. 1999).
Even though the initial events of the eye organogenesis are homologous in flies and vertebrates, the structural and anatomical differences (those discussed in previous sections) arise due to extremely complicated genetic networks, controlled by signaling events which are different in terms of spatiotemporal profiles, yet are governed similarly in the later stages of development which lead to formation of a three-dimensional eye.
Signaling aspect of cell–cell communication plays a major role in both vertebrate and Drosophila eye development. Drosophila equivalents of TGF-β, Sonic Hedgehog, JNK, JAK STAT, EGFR, and Notch pathways have been widely studied in eye development as early as axes determination until sculpting the final organ shape (Greenwood and Struhl 1999; Roessler et al. 1996) (Fig. 4).
Concluding Remarks
Eye development is vast and has been studied widely to understand the processes of organogenesis and physiology by more researchers than we can think of. In the entire past century, the developmental biologists have elucidated basic framework of eye organogenesis in early and later stages, to understand the regulation and execution of these processes. With this framework aided with newer technologies such as 5D light sheet microscopy, newer forms of genetic manipulation techniques, and genome projects in Drosophila as well as vertebrate models, a converge understanding of regulators of eye development is being paved, which will aid the pre-existing knowledge to extrapolate the analogies between the two.
References
Agi E, Langen M, Altschuler SJ, Wu LF, Zimmermann T, Hiesinger PR (2014) The evolution and development of neural superposition. Journal of Neurogen 28(3–4). https://doi.org/10.3109/01677063.2014.922557
Azuma N, Hirakiyama A, Inoue T, Asaka A, Yamada M (2000) Mutations of a human homologue of the Drosophila eyes absent gene (EYA1) detected in patients with congenital cataracts and ocular anterior segment anomalies. Hum Mol Genet 9(3):363–366
Baccus SA, Ölveczky BP, Manu M, Meister M (2008) A retinal circuit that computes object motion. J Neurosci 28(27):6807–6817
Baden T, Berens P, Franke K, Rosón MR, Bethge M, Euler T (2016) The functional diversity of retinal ganglion cells in the mouse. Nature 529(7586):345
Baker BS, Carpenter AT, Ripoll P (1978) The utilization during mitotic cell division of loci controlling meiotic recombination and disjunction in Drosophila melanogaster. Genetics 90(3):531–578
Bonini NM, Leiserson WM, Benzer S (1993) The eyes absent gene: genetic control of cell survival and differentiation in the developing Drosophila eye. Cell 72(3):379–395
Borsani G, DeGrandi A, Ballabio A, Bulfone A, Bernard L, Banfi S, Gattuso C, Mariani M, Dixon M, Donnai D, Metcalfe K (1999) EYA4, a novel vertebrate gene related to Drosophila eyes absent. Hum Mol Genet 8(1):11–23
Borst A (2009) Drosophila’s view on insect vision. Curr Biol 19(1):R36–R47
Cajal S, Sanchez D (1915) Contribucion al conocimiento de los centros nerviosos del los insectos. Trab lab invest biol, 1983 74(1–4):1–164
Caubit X, Thangarajah R, Theil T, Wirth J, Nothwang HG, Rüther U, Krauss S (1999) Mouse Dac, a novel nuclear factor with homology to Drosophila dachshund shows a dynamic expression in the neural crest, the eye, the neocortex, and the limb bud. Dev Dyn 214(1):66–80
Chaffiol A, Ishii M, Cao Y, Mangel SC (2017) Dopamine regulation of GABAA receptors contributes to light/dark modulation of the ON-cone bipolar cell receptive field surround in the retina. Curr Biol 27(17):2600–2609
Chang T, Mazotta J, Dumstrei K, Dumitrescu A, Hartenstein V (2001) Dpp and Hh signaling in the Drosophila embryonic eye field. Development 128(23):4691–4704
Chen Y, Riese MJ, Killinger MA, Hoffmann FM (1998) A genetic screen for modifiers of Drosophila decapentaplegic signaling identifies mutations in punt, Mothers against dpp and the BMP-7 homologue, 60A. Development 125(9):1759–1768
Chen R, Halder G, Zhang Z, Mardon G (1999) Signaling by the TGF-beta homolog decapentaplegic functions reiteratively within the network of genes controlling retinal cell fate determination in Drosophila. Development 126(5):935–943
Cheyette BN, Green PJ, Martin K, Garren H, Hartenstein V, Zipursky SL (1994) The Drosophila sine oculis locus encodes a homeodomain-containing protein required for the development of the entire visual system. Neuron 12(5):977–996
Collinson JM, Hill RE, West JD (2000) Different roles for Pax6 in the optic vesicle and facial epithelium mediate early morphogenesis of the murine eye. Development 127(5):945–956
Czerny T, Halder G, Kloter U, Souabni A, Gehring WJ, Busslinger M (1999) twin of eyeless, a second Pax-6 gene of Drosophila, acts upstream of eyeless in the control of eye development. Mol Cell 3(3):297–307
Gallardo ME, Lopez-Rios J, Fernaud-Espinosa I, Granadino B, Sanz R, Ramos C, Ayuso C, Seller MJ, Brunner HG, Bovolenta P, de Córdoba SR (1999) Genomic cloning and characterization of the human homeobox gene SIX6 reveals a cluster of SIX genes in chromosome 14 and associates SIX6 hemizygosity with bilateral anophthalmia and pituitary anomalies. Genomics 61(1):82–91
Gehring W (1967) Clonal analysis of determination dynamics in cultures of imaginal disks in Drosophila melanogaster. Dev Biol 16(5):438–456
Glaser T, Walton DS, Maas RL (1992) Genomic structure, evolutionary conservation and aniridia mutations in the human PAX6 gene. Nat Genet 2(3):232
Gollisch T, Meister M (2010) Eye smarter than scientists believed: neural computations in circuits of the retina. Neuron 65(2):150–164
Grainger RM (1992) Embryonic lens induction: shedding light on vertebrate tissue determination. Trends Genet 8(10):349–355
Green P, Hartenstein AY, Hartenstein V (1993) The embryonic development of the Drosophila visual system. Cell Tissue Res 273(3):583–598
Greenwood S, Struhl G (1999) Progression of the morphogenetic furrow in the Drosophila eye: the roles of Hedgehog, Decapentaplegic and the Raf pathway. Development 126(24):5795–5808
Grindley JC, Davidson DR, Hill RE (1995) The role of Pax-6 in eye and nasal development. Development 121(5):1433–1442
Halder G, Callaerts P, Gehring WJ (1995) New perspectives on eye evolution. Curr Opin Genet Dev 5(5):602–609
Halder G, Callaerts P, Flister S, Walldorf U, Kloter U, Gehring WJ (1998) Eyeless initiates the expression of both sine oculis and eyes absent during Drosophila compound eye development. Development 125(12):2181–2191
Hammond KL, Hanson IM, Brown AG, Lettice LA, Hill RE (1998) Mammalian and Drosophila dachshund genes are related to the Ski proto-oncogene and are expressed in eye and limb. Mech Dev 74(1):121–131
Haynie JL, Bryant PJ (1986) Development of the eye-antenna imaginal disc and morphogenesis of the adult head in Drosophila melanogaster. J Exp Zool 237(3):293–308
Heanue TA, Reshef R, Davis RJ, Mardon G, Oliver G, Tomarev S, Lassar AB, Tabin CJ (1999) Synergistic regulation of vertebrate muscle development by Dach2, Eya2, and Six1, homologs of genes required for Drosophila eye formation. Genes Dev 13(24):3231–3243
Heberlein U, Wolff T, Rubin GM (1993) The TGFβ homolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina. Cell 75(5):913–926
Huang YS, Ku HY, Tsai YC, Chang CH, Pao SH, Sun YH, Chiou A (2017) 5D imaging via light sheet microscopy reveals cell dynamics during the eye-antenna disc primordium formation in Drosophila. Sci Rep 7:44945
Jarman AP (2000) Developmental genetics: vertebrates and insects see eye to eye. Curr Biol 10(23):R857–R859
Jürgens G, Lehmann R, Schardin M, Nüsslein-Volhard C (1986) Segmental organisation of the head in the embryo of Drosophila melanogaster. Rouxs Arch Dev Biol 195(6):359–377
Kozmik Z, Pfeffer P, Kralova J, Paces J, Paces V, Kalousova A, Cvekl A (1999) Molecular cloning and expression of the human and mouse homologues of the Drosophila dachshund gene. Dev Genes Evol 209(9):537–545
Kulkarni A, Ertekin D, Lee CH, Hummel T (2016) Birth order dependent growth cone segregation determines synaptic layer identity in the Drosophila visual system. elife 5:e13715
Kumar JP (2018) The fly eye: through the looking glass. Dev Dyn 247(1):111–123
Mardon G, Solomon NM, Rubin GM (1994) Dachshund encodes a nuclear protein required for normal eye and leg development in Drosophila. Development 120(12): 3473–3486.
Masland RH (2001) The fundamental plan of the retina. Nat Neurosci 4(9):877
Masland RH (2012) The neuronal organization of the retina. Neuron 76(2):266–280. https://doi.org/10.1016/j.neuron.2012.10.002
Meinertzhagen IA, O’neil SD (1991) Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. J Comp Neurol 305(2):232–263
Morante J, Desplan C (2008) The color-vision circuit in the medulla of Drosophila. Curr Biol 18(8):553–565
Münch TA, Da Silveira RA, Siegert S, Viney TJ, Awatramani GB, Roska B (2009) Approach sensitivity in the retina processed by a multifunctional neural circuit. Nat Neurosci 12(10):1308
Namba R, Minden JS (1999) Fate mapping of Drosophila embryonic mitotic domain 20 reveals that the larval visual system is derived from a subdomain of a few cells. Dev Biol 212(2):465–476
Ohto H, Kamada S, Tago K, Tominaga SI, Ozaki H, Sato S, Kawakami K (1999) Cooperation of six and eya in activation of their target genes through nuclear translocation of Eya. Mol Cell Biol 19(10):6815–6824
Ohto H, Takizawa T, Saito T, Kobayashi M, Ikeda K, Kawakami K (2002) Tissue and developmental distribution of Six family gene products. Int J Dev Biol 42(2):141–148
Otsuna H, Ito K (2006) Systematic analysis of the visual projection neurons of Drosophila melanogaster. I. Lobula-specific pathways. J Comp Neurol 497(6):928–958
Ouweneel WJ (1970) Normal and abnormal determination in the imaginal discs of Drosophila, with special reference to the eye discs. Acta Embryol Exp 1:95
Pak WL (2010) Why Drosophila to study phototransduction? J Neurogenet 24:55–66
Parker AR (2009) On The Origin of Optics. Opt Laser Technol 43(2):323–329. https://doi.org/10.1016/J.Optlastec.2008.12.020
Pei YF, Rhodin JA (1970) The prenatal development of the mouse eye. Anat Rec 168(1):105–125
Piatigorsky J, Wistow GJ (1989) Enzyme/crystallins: gene sharing as an evolutionary strategy. Cell 57(2):197–199
Prosser J, van Heyningen V (1998) PAX6 mutations reviewed. Hum Mutat 11(2):93–108
Quinn JC, West JD, Hill RE (1996) Multiple functions for Pax6 in mouse eye and nasal development. Genes Dev 10(4):435–446
Quiring R, Walldorf U, Kloter U, Gehring WJ (1994) Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in humans. Science 265(5173):785–789
Ready DF, Hanson TE, Benzer S (1976) Development of the Drosophila retina, a neurocrystalline lattice. Dev Biol 53(2):217–240
Roessler E, Belloni E, Gaudenz K, Jay P, Berta P, Scherer SW, Tsui LC, Muenke M (1996) Mutations in the human Sonic Hedgehog gene cause holoprosencephaly. Nat Genet 14(3):357
Salcedo E, Huber A, Henrich S, Chadwell LV, Chou WH, Paulsen R, Britt SG (1999) Blue-and green-absorbing visual pigments of Drosophila: ectopic expression and physiological characterization of the R8 photoreceptor cell-specific Rh5 and Rh6 rhodopsins. J Neurosci 19(24):10716–10726
Sanes JR, Zipursky SL (2010) Design principles of insect and vertebrate visual systems. Neuron 66(1):15–36
Sinakevitch I, Douglass JK, Scholtz G, Loesel R, Strausfeld NJ (2003) Conserved and convergent organization in the optic lobes of insects and isopods, with reference to other crustacean taxa. J Comp Neurol 467(2):150–172
Singh A, Choi KW (2003) Initial state of the Drosophila eye before dorsoventral specification is equivalent to ventral. Development 130(25):6351–6360
Singh A, Shi X, Choi KW (2006) Lobe and Serrate are required for cell survival during early eye development in Drosophila. Development 133(23):4771–4781
Singh A, Tare M, Puli OR, Kango-Singh M (2012) A glimpse into dorso-ventral patterning of the Drosophila eye. Dev Dyn 241(1):69–84
Singh A, Gogia N, Chang, CY, Sun, YH (2019) Proximal fate marker homothorax marks the lateral extension of stalk-eyed fly Cyrtodopsis whitei. Genesis 57:e23309. https://doi.org/10.1002/dvg.23309
Stavenga DG, Foletti S, Palasantzas G, Arikawa K (2005) Light on the moth-eye corneal nipple array of butterflies. Proc R Soc B Biol Sci 273(1587):661–667
Takemura SY, Lu Z, Meinertzhagen IA (2008) Synaptic circuits of the Drosophila optic lobe: the input terminals to the medulla. J Comp Neurol 509(5):493–513
Ton CC, Hirvonen H, Miwa H, Weil MM, Monaghan P, Jordan T, van Heyningen V, Hastie ND, Meijers-Heijboer H, Drechsler M, Royer-Pokora B (1991) Positional cloning and characterization of a paired box-and homeobox-containing gene from the aniridia region. Cell 67(6):1059–1074
Toy J, Yang JM, Leppert GS, Sundin OH (1998) The optx2 homeobox gene is expressed in early precursors of the eye and activates retina-specific genes. Proc Natl Acad Sci 95(18):10643–10648
Tsukamoto Y, Omi N (2013) Functional allocation of synaptic contacts in microcircuits from rods via rod bipolar to aII amacrine cells in the mouse retina. J Comp Neurol 521(15):3541–3555
Vogt DW, Anderson DF (1964) Studies on bovine ocular squamous carcinoma (“cancer eye”) XV. Heritability of susceptibility. J Hered 55(3):133–135
Wallis DE, Roessler E, Hehr U, Nanni L, Wiltshire T, Richieri-Costa A, Gillessen-Kaesbach G, Zackai EH, Rommens J, Muenke M (1999) Mutations in the homeodomain of the human SIX3 gene cause holoprosencephaly. Nat Genet 22(2):196
Walther CL, Gruss PE (1991) Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113(4):1435–1449
Wawersik S, Purcell P, Rauchman M, Dudley AT, Robertson EJ, Maas R (1999) BMP7 acts in murine lens placode development. Dev Biol 207(1):176–188
Weismann A (1864) Die nachembryonale Entwicklung der Musciden nach Beobachtungen an Musca vomitoria und Sarcophaga carnaria Zeit. Wiss Zool 14:187–336
Wolff TA, Ready DF (1991) The beginning of pattern formation in the Drosophila compound eye: the morphogenetic furrow and the second mitotic wave. Development 113(3):841–850
Xu PX, Woo I, Her H, Beier DR, Maas RL (1997) Mouse Eya homologues of the Drosophila eyes absent gene require Pax6 for expression in lens and nasal placode. Development 124(1):219–231
Yao X, Cafaro J, McLaughlin AJ, Postma FR, Paul DL, Awatramani G, Field GD (2018) Gap Junctions Contribute to Differential Light Adaptation across Direction-Selective Retinal Ganglion Cells. Neuron 100(1):216–228
Younossi-Hartenstein A, Tepass U, Hartenstein V (1993) Embryonic origin of the imaginal discs of the head of Drosophila melanogaster. Rouxs Arch Dev Biol 203(1–2):60–73
Zimmerman JE, Bui QT, Steingrímsson E, Nagle DL, Fu W, Genin A, Spinner NB, Copeland NG, Jenkins NA, Bucan M, Bonini NM (1997) Cloning and characterization of two vertebrate homologs of the Drosophila eyes absent gene. Genome Res 7(2):128–141
Zuber ME, Perron M, Philpott A, Bang A, Harris WA (1999) Giant eyes in Xenopus laevis by overexpression of XOptx2. Cell 98(3):341–352
Acknowledgement
Authors would like to thank Ms. Tripti Misra for arranging and commenting on the manuscript, in addition to Mr. Bhavsar to help with figure drawings. We apologize to the authors and publications that we could not include in our references.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2020 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Rai, A., Narwal, S., Kanodia, H., Tare, M. (2020). Eye for an Eye: A Comparative Account on Compound Eye of Drosophila melanogaster with Vertebrate Eye. In: Singh, A., Kango-Singh, M. (eds) Molecular Genetics of Axial Patterning, Growth and Disease in Drosophila Eye. Springer, Cham. https://doi.org/10.1007/978-3-030-42246-2_12
Download citation
DOI: https://doi.org/10.1007/978-3-030-42246-2_12
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-42245-5
Online ISBN: 978-3-030-42246-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)