© 2003 by The Society for Integrative and Comparative Biology
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Evolution of Insect Eye Development: First Insights from Fruit Fly, Grasshopper and Flour Beetle1
1 Department of Biological Sciences, Wayne State University, 5047 Gullen Mall, Detroit, Michigan 48202
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INTRODUCTIONThe molecular genetic dissection of Drosophila eye development led to the exciting discovery of a surprisingly large panel of genes and gene activities, which are functionally conserved across phyla. Little effort has yet been made towards pinpointing non-conserved gene functions in the developing Drosophila eye. This neglects the fact that Drosophila visual system development is a highly derived process. The comparative analysis of Drosophila eye development within insects can be expected to enhance resolution and accuracy of between phyla comparisons of eye development, and to reveal molecular developmental changes that facilitated the evolutionary transition from hemimetabolous to holometabolous insect development. Here we review aspects of early Drosophila eye development, which are likely to have diverged from the situation in more primitive insects, as indicated by results from work in the flour beetle Tribolium castaneum and the grasshopper Schistocerca americana.
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INTRODUCTION |
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The power of biological model systems equals the ease of genetic analysis multiplied by applicability to human biology. The fruit fly Drosophila melanogaster has performed beyond expectation under this equation. Originally chosen for reasons of affordability and short generation time rather than similarity to vertebrate physiology, the analysis of the complete Drosophila genome delivered ultimate proof that this model species also positions usefully close to humans on the tree of life if shared genes and gene functions are taken as measure of relatedness (Rubin et al., 2000
). The surprising evolutionary insights that emanated from the molecular dissection of Drosophila compound eye development constitute a paradigm case of radical change of comparative perspective. Considering the fundamental differences between the Drosophila compound eye and the vertebrate lens eye, an independent origin of insect and vertebrate visual organs seemed certain (Salvini-Plawen and Mayr, 1977). This premolecular view was revolutionized by the discovery in Walter Gehring's laboratory that the orthologs of the paired class transcription factor Pax6 are essential for eye development in both fly and vertebrates (Quiring et al., 1994). Subsequent studies revealed that homologs of three equally conserved gene families eyes absent (eya), sine oculis (so) and dachshund (dac) interact with Pax6 in an evolutionarily conserved eye specification regulatory network (for review see Desplan, 1997; Pappu and Mardon, 2002). The finding of similarities in the function of the proneural transcription factor atonal (ato) and the signaling molecule hedgehog (hh) in the developing retina of flies and vertebrates raised the possibility that the conservation of animal eye development extends to processes downstream of eye specification (Kumar, 2001; Brown et al., 2001; Neumann and Nuesslein-Volhard, 2000).
The nature of Drosophila eye development conservation has been a topic of lively discussion (Halder et al., 1995; Hanson and Van Heyningen, 1995; Gehring, 1996; Tomarev, 1997; Kumar, 2001; Pichaud et al., 2001; Pichaud and Desplan, 2002). Less attention has been paid to the fact that Drosophila eye development also offers the opportunity to unravel molecular developmental changes underlying the emergence of evolutionary novelty. Drosophila represents one of the most derived modes of insect eye development to the eyes of an entomologist (Fig. 1). This is in part due to the derived life cycle and in part to unique morphological modifications of the juvenil instars. As is typical for holometabolous insects, the fruitfly develops through a series of specialized postembryonic growth stages. These larval instars lack most elements of the adult body plan including the compound eyes. The complex transformation to adult morphology begins in the last larval instar and completes during the resting stage of the pupa. The development of the adult Drosophila eye is thus a postembryonic process. In primitive insects, however, much of the adult retina develops already during embryogenesis (Fig. 1). The immature instars or nymphs of hemimetabolous insects such as grasshopper or cockroach for instance are born with adult like morphology. Elaboration of the adult morphology during the final nymphal molt requires only the extension of wings in addition to differentiation of functional genitalia. The first instar nymph possesses a pair of fully functional compound eyes, which are enlarged between the subsequent growth molts and maintained into the adult. Morphological and molecular data firmly establish that holometabolous development evolved from within hemimetabolous insects (Kristensen, 1995). The postembryonic mode of Drosophila eye development is thus clearly an evolutionarily derived process.
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Evolutionary change of morphology requires change of developmental programs (Carroll, 1994
). Evidently, the evolution of holometabolous insects must have involved modifications of embryonic development to generate the derived morphology of the larva. It is also reasonable to assume that the postembryogenic differentiation of adult structures starting from the larval body plan involved modifications of ancestrally embryonic differentiation processes. Thus, the evolutionary transition from embryonic to postembryonic eye development most likely involved not only a temporal shift of the onset of adult retina differentiation, but also considerable modifications of embryonic and postembryonic visual system development. The extent to which the deeply conserved molecular genetic control mechanisms of Drosophila eye development are embedded in derived patterning mechanisms is unclear. This is because our knowledge of insect eye development outside the genus Drosophila is fairly limited. Accounts on eye development in insect species other than Drosophila are scattered (Meinertzhagen, 1973; Bate, 1978; Trujillo-Cenoz, 1985; Egelhaaf, 1988; Melzer and Paulus, 1994; Friedrich et al., 1996; Champlin and Truman, 1998). A major focus has been the comparison of the sequence of cell differentiation events in the developing retina, which is highly conserved in insects and crustaceans (Melzer et al., 2000; Hafner and Tokarski, 2001). This review discusses first evidence for evolutionary divergence of molecular genetic patterning events, which lead up to the onset of differentiation of the compound eye retina in Drosophila. Examples will be drawn from ongoing comparative analyses in the American desert locust Schistocerca americana, a hemimetabolous insect, and the flour beetle Tribolium castaneum, a primitive holometabolous insect.
Drosophila, Tribolium and Schistocerca: Three ways to make an insect eye
Drosophila represents one of the most complex modes of insect compound eye development (for review see Wolff and Ready, 1993). First complications stem from the fact that the Drosophila larva is acephalic. It lacks head appendages and is furnished with an internalized head skeleton instead (Fig. 1). As a consequence, the larval head components are replaced with newly differentiated adult head capsule tissues during postembryonesis. The cuticle skeleton of the adult head develops from specialized ectodermal sacs, the imaginal discs. These may be considered secondary embryonic fields that are set aside during early embryogenesis and remain buried deep inside the body during larval development. The compound eye retina develops from the eye-antennal imaginal disc, which is a derivative of the embryonic visual primordium (Fig. 2A). Only little developed at the beginning of postembryogenesis the eye-antennal imaginal disc proceeds through continuous growth and differentiation during larval development. By the second larval instar, the anterior part, which will give rise to the antenna, can be morphologically discriminated from the posterior part, which will form the retina and additional head cuticle areas. Close to middle of the third and last larval instar, retina differentiation starts at the posterior margin of the eye disc. This process is marked by formation of the morphogenetic furrow, which refers to the front of differentiation where cells are uniformly shorter and distally constricted forming a conspicuous indentation along the dorsoventral axis of the eye disc. The furrow moves from its posterior start point towards anterior (Fig. 2D). Posterior to the furrow, ommatidial preclusters emerge in a regular array anticipating the regularity of the adult retina. Photoreceptor cells join the ommatidial preclusters first, followed by cone cells and pigment cells. This early phase of retina cell determination and differentiation continues until the furrow has reached its final destination at about 10 hours after pupation when the eye disc everts. Once the entire eye field has been established, the retina cells undergo terminal differentiation in a concerted manner. Hallmarks of this process are the elimination of surplus cells by apoptosis, synthesis of screening pigments and elaboration of the photoreceptor cell rhabdomeres. Approximately two thirds of the posterior eye disc proper differentiates as retina while the anterior third and parts of the peripodial membrane, which is the second tissue layer of the sac-like disc, develop into adjacent head cuticle elements (Haynie and Bryant, 1986).
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Eye imaginal disc formation as seen in Drosophila is not an obligatory feature of postembryonic eye development in holometabolous insects. More basal dipteran and holometabolous species develop through a eucephalic larva, which carries a fully developed head capsule equipped with antennal and mouthpart appendages. The larva of the flour beetle Tribolium castaneum exemplifies this level of evolutionary organization (Fig. 1). In this case, metamorphosis is significantly less dramatic. The differentiation of the adult body plan proceeds through reinitiated growth and terminal differentiation of larval structures, which from this perspective function as adult organ primordia. The adult antenna for instance develops via dramatic growth and further differentiation of the larval antenna. The adult Tribolium retina, however, is not formed by further differentiation of the larval eyes. It seems to develop de novo in a region of the late larval head, which corresponds to the future field of the retina in the adult head capsule. This ectodermal tissue compartment has been termed "eye placode" (Fig. 2E) (Marshall, 1928
; Friedrich et al., 1996; Friedrich and Benzer, 2000). The beginning of Tribolium retina differentiation is marked by the initiation of the morphogenetic furrow at the posterior margin of the eye placode. The morphogenetic furrow passes through the eye placode in anterior direction, coming to halt shortly before the antenna. The timing of Tribolium retina differentiation corresponds very closely to that in Drosophila (Fig. 1). The progression of the morphogenetic furrow starts during the second half of the last larval instar and continuous through approximately the first third of pupation after which terminal differentiation initiates. It is important to note that the Tribolium eye placode area becomes fully elaborated in the embryo together with all other essential compartments of the adult head (Fig. 2B). In the more primitive Tribolium, adult head compartment and for the most part organ primordia formation have remained embryonic. It is separated in time from the postembryonic differentiation of the adult retina. This marks a fundamental difference to the continuous postembryonic morphogenesis of the Drosophila head from internalized imaginal discs, and the integration of Drosophila retina differentiation into this derived process.
Eye development in hemimetabolous insects such as the grasshopper Schistocerca americana is a repetitive multi-step process which starts in the embryo and extends through postembryogenesis (Fig. 1) (Anderson, 1978; Friedrich and Benzer, 2000). Almost one third of the adult Schistocerca compound eye retina is of embryonic origin. This embryonic fraction is formed from the ectoderm of the lateral-most tissue compartments of the embryonic head, the eye lobes (Fig. 2C). The morphogenetic furrow initiates in the posterior margin of the eye lobe ectoderm shortly before 35% of embryogenesis. With the morphogenetic furrow progressing anteriorly, the embryonic retina continues to extend in anterior direction throughout much of the second half of embryogenesis, which however is also characterized by the terminal differentiation of the retina. Most of the eye field of the first instar nymph is thus fully differentiated and functional. Except for the anterior margin where cell proliferation and differentiation continuously reinitiate between the postembryonic growth molts thereby enlarging the embryonic retina field to the size of the adult retina in several postembryonic increments (Figs. 1 and 2F) (Anderson, 1978).
The evolution of postembryonic eye development must have required the elaboration of mechanisms which prevent the onset of adult retina differentiation in the embryo, maintain the prospective retina field during early postembryogenesis, and coordinate the postembryogenetic differentiation of the adult retina with the complex process of metamorphosis. These changes of development represent ground state changes as they are prerequisite for the postembryonic development of the compound eye retina in holometabolous species in general. Additional modifications must have evolved in the lineage leading to Drosophila, which, as indicated, concerned the postembryonic development of the prospective retinal field and the coordination of this process with the de novo development of the other adult head primordia in the eye-antennal imaginal disc. Yet further modifications of embryonic visual system development are likely to have been enforced in Drosophila by the evolution of its extreme mode of short germ development in combination with the evolution of the acephalic larval head morphology (Melzer and Paulus, 1989). It is thus not surprising that the molecular control of Drosophila eye development differs from that in more primitive species at numerous steps preceding the final differentiation of the eye field.
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PATTERNING OF THE EMBRYONIC VISUAL ANLAGE |
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Specification of the precursor embryonic tissue which gives rise to the visual system is the first step in the sequence of events leading to the formation of the insect eye. In Drosophila, all visual system components map to a single unpaired primordium straddling the dorsal midline in the anterior head region of the blastoderm embryo, which is traditionally considered the nonsegmental tip of the embryo (acron) and in addition includes the anlagen for the first brain neuromer, the protocerebrum (Green et al., 1993
; Dumstrei et al., 1998; Namba and Minden, 1999). The Drosophila visual primordium is molecularly defined by expression of the homeobox gene so (Cheyette et al., 1994; Serikaku and O'Tousa, 1994; Chang et al., 2001). Homologs of so (Six3/6) are also involved in specifying the visual primordium in other animal phyla (Oliver et al., 1995; Jean et al., 1999). While the transcriptional code for Drosophila visual primordium specification seems highly conserved, the mechanisms responsible for its initial spatial regulation may be of more recent evolutionary origin. The expression of so in the visual primordium depends on activation by the TGF-ß signaling factor decapentaplegic (dpp), which is expressed in a dorsoventral gradient in the early Drosophila blastoderm embryo (Chang et al., 2001). Maximal Dpp levels in the dorsal midline of the embryo initiate expression of the HOX-3 orthologous transcription factor zerknuellt (zen) which represses so expression along the dorsal midline (Fig. 3). At the same time, lower Dpp levels continue to activate so expression along the lateral sides of the embryo. It has been noted that the resulting split of the visual anlage resembles the morphogenesis of the vertebrate anterior plate (Chang et al., 2001). In this case, however, homologs of the signaling factor gene hh, induce the median split of the anterior brain anlage (Ekker et al., 1995).
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A possible explanation for this discrepancy is that the long germ insect Drosophila exhibits considerable differences in the formation of the embryonic anlagen compared to the ancestral mode of short germ development. This raises the possibility that evolutionarily derived anterior head patterning mechanisms in Drosophila replaced ancestral mechanisms. Indeed, two lines of evidence from anterior patterning gene expression in primitive short germ insects such as Tribolium and Schistocerca suggest that midline patterning of the Drosophila head is controlled by derived mechanisms (Fig. 3). In both of these species zen is expressed in the extra-embryonic serosa and amnionic membrane tissue but not in the germband proper (Falciani et al., 1996
; Dearden et al., 2000). The peripheral location of this expression domain excludes an involvement of zen in patterning the embryonic midline of these species. Furthermore, the expression of dpp overlaps with that of zen in the serosa and amnionic membrane of Tribolium and Schistocerca. This suggests that the activation of zen by dpp is conserved during extraembryonic tissue specification (Sanchez-Salazar et al., 1996; Dearden and Akam, 2001). The spatial regulation of its expression pattern however makes it seem unlikely that dpp is involved in midline patterning using alternative transcriptional mediators.
Second, genes involved in patterning the anterior Drosophila head such as tailless (tll), orthodenticle (otd), and the segmentation gene wingless (wg) are typically expressed in circumferential domains straddling the dorsal ectoderm midline like so (Nagy and Carroll, 1994; Chang et al., 2001). With the onset of gastrulation, these circumferential stripes break up into isolated expression elements. In most cases, expression ceases in the dorsal midline reminiscent of dorsal midline so repression by dpp/zen. In Tribolium however the earliest detectable blastoderm expression patterns of wg, tll, and otd are already split in the dorsal midline (Nagy and Carroll, 1994; Li et al., 1996; Schroder et al., 2000). The same is true for the expression of wg in the orthopteran species Acheta domesticus and Schistocerca gregaria (Niwa et al., 2000; Dearden and Akam, 2001). Taken together, these data support the existence of ancestral midline patterning mechanisms that might have been strongly modified or lost during Drosophila evolution.
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RETINAL FATE COMMITMENT (I): EYE VERSUS ANTENNA |
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The Drosophila visual system consists of several components. The information received by the regular sensory array of the facetted retina is processed in the optic neuropil layers lamina, medulla, and lobula, which together constitute the optic lobe. In addition, the fruit fly possesses three ocelli, comparatively simple photosensory organs that are centered between the compound eyes at the dorsal midline of adult head, and an extra set of simple larval eyes, the Bolwig organs. Except for the ocelli, the tissues of all Drosophila visual system components derive from compartmentalization of the early embryonic visual anlage at stage 12 of Drosophila embryonic development (Fig. 2A). At the stage of visual primordium partitioning, the population of cells, which will give rise to the primordium of the adult retina, the eye imaginal disc, is characterized by specific expression of the master regulatory gene ey (Chang et al., 2001
; Kumar and Moses, 2001c). This would suggest early commitment of the Drosophila eye disc, in line with the fate mapping supported view that the adult Drosophila retina is determined during embryogenesis (Postlethwait and Schneiderman, 1971; Younossi-Hartenstein et al., 1993). However, partitioning of precursor tissue may not be correlated with terminal commitment for organ fate. The differentiation of the Drosophila retina is the endpoint of a series of discrete stages of tissue commitment. This was discovered studying of the role of Notch (N) and Epidermal growth factor receptor (Egfr) signaling during early eye-antennal disc development, which revealed that the posterior part of the eye-antennal imaginal disc remains competent to adopt antennal fate until the second half of the second larval instar (Fig. 1) (Kumar and Moses, 2001a). At this stage, the commitment decision of eye versus antenna fate is under antagonistic control of the two signaling pathways with N signaling promoting retina fate versus Egfr signaling promoting antenna fate. Consistent with the experimental evidence for postembryonic determination of the retina field primordium, the regulatory genes essential for Drosophila retina development are not coexpressed in the eye-antennal disc before the second larval instar. Induction of Drosophila retinal fate results from the concerted action of seven transcriptional regulators: the recently duplicated Drosophila Pax6 orthologs ey and twin of eyeless (toy), the related paired domain protein eye gone (eyg), and the transcription factors dac, eya, so and optix (reviewed in Kumar, 2001; Pappu and Mardon, 2002). Only toy and eyg are coexpressed with ey in the eye-antennal disc primordium following compartmentalization of the embryonic visual anlage (Kumar and Moses, 2001c). This step controls the specification of the retinal precursor tissue, which is followed by postembryonic determination. In a consistent manner, also the delay of antenna primordium determination correlates with absence of the antenna fate specifying transcription factor distal-less (dll) in the embryonic antennal anlage (Kumar and Moses, 2001a).
From a comparative perspective it is important to note that the absence of adult retina and antenna differentiation in the Drosophila embryo correlates with the lack of expression of transcription factors, which are essential for the determination of the retina and antenna primordia. In non-holometabolous insects such as Schistocerca, the primordia of both the adult antenna and eye are formed during embryonic development (Fig. 2C). This implies that all of the required determination genes need to be expressed already in the respective embryonic anlagen. Transcription factors, which are known to function in Drosophila antenna determination such as dll, spalt-major (salm) and extradenticle (exd) (Dong et al., 2002), are indeed expressed in the embryonic grasshopper antenna (Friedrich, unpublished observation). One prediction from the Drosophila model is therefore that also the eye determination genes are coexpressed in the posterior eye lobe margin of the grasshopper prior to the initiation of retina differentiation. Preliminary analyses of eya and so expression during grasshopper embryonic development have yielded results that are consistent with such scenario (Dong and Friedrich, unpublished).
Hypothesis building regarding the onset of eye determination transcription factor coexpression during visual system development in Tribolium is less straightforward. Two scenarios are conceivable. Evidently, the primordia of the adult antennae are formed during embryogenesis in the form of the larval antennae, which also holds for most other head structures in the eucephalic Tribolium (Fig. 2B). By analogy, the compound eye retina primordium, i.e., the eye placode, may also be determined in the embryo but prevented from initiating differentiation. The determination step may involve coexpression of the retinal determination genes in the embryonic retinal primordium. However, morphological or molecular evidence for embryonic determination of the Tribolium eye placode is yet missing. Alternatively, the shift of retina determination network gene coexpression into postembryogenesis seen in Drosophila may represent a mechanism, which evolved early in holometabolous insects to preclude embryonic differentiation of adult retina. For this hypothesis to hold true, the members of the Tribolium eye specification transcription factor network should not be coexpressed during embryonic development but in the eye placode during postembryonic development (Fig. 1). The comprehensive analysis of eye determination gene expression in Tribolium and Schistocerca will provide the data necessary for the correct evolutionary interpretation of postembryonic retina determination in Drosophila.
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AXIS AND COMPARTMENT SPECIFICATION |
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The Drosophila eye-antennal imaginal disc proceeds through continuous patterning and growth during larval development. Fundamental patterning steps concern the establishment of the anteroposterior and dorsoventral axes (Lee and Treisman, 2001
). In addition, the retina field is divided into dorsal and ventral compartments, which meet exactly along the midline of the disc forming a border that has been termed the equator. In developmental terms, the equator is an N signaling based organizing center, which stimulates growth of the eye disc prior to the onset of retina differentiation, and provides signals necessary for planar cell polarity patterning in the differentiating retina (Cho and Choi, 1998; Dominguez and de Celis, 1998; Papayannopoulos et al., 1998; Reifegerste and Moses, 1999; Cho et al., 2000). Morphologically, the Drosophila equator becomes manifest by a 90 degree rotation of the developing ommatidia, which occurs in mirror image orientation in the dorsal and ventral half of the retina field (Fig. 4B) (Dietrich, 1909). The dorsoventral compartmentalization of the Drosophila retina field also affects early patterning and growth of the eye disc. Genetic ablation of the Lobe gene for instance leads to ventral specific loss of retina growth (Chern and Choi, 2002). Loss of homothorax (hth) gene activity leads to ectopic retina differentiation in the ventral but not dorsal compartment of the eye disc (Pichaud and Casares, 2000). The zinc finger transcription factor teashirt (tsh) represses retina differentiation in the ventral compartment but promotes retina differentiation in the dorsal compartment (Singh et al., 2002).
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The occurrence of similar dorsoventral compartment pattern elements in the retina of other arthropod species as well as the general need for tissue growth in the developing retina would lead one to expect that formation of the equatorial organizing center by dorsoventral compartment formation is a conserved aspect of Drosophila eye disc development (Friedrich et al., 1996
). This hypothesis can be tested as the gene network involved in dorsoventral compartment formation is well understood (Cho and Choi, 1998; Dominguez and de Celis, 1998; Papayannopoulos et al., 1998; Cho et al., 2000). One of the first steps involves the dorsal compartment specific activation of wg expression by the transcription factor pannier (pnr) (Maurel-Zaffran and Treisman, 2000). Wg in turn activates expression of the homeobox transcription factor mirror (mirr) the function of which is to suppress the expression of fringe (fng) in the dorsal part of the disc (Yang et al., 1999). As a consequence, fng expression is restricted to the ventral compartment. This leads to specific activation of N signaling along the midline where fng enhances the activation of N by its ligand Delta (Dl) while suppressing N activation by the second N ligand Serrate (Ser) in the ventral part of the disc. In summary, dorsal expression of pnr, wg and mirr, versus ventral expression of fng are essential elements of dorsoventral compartment formation in the Drosophila eye disc (Fig. 4).
Interestingly, wg is not expressed in a dorsalized manner throughout development of the early grasshopper embryonic retina although the polar expression of wg at the anterior retina margin is conserved (Fig. 6) (Friedrich and Benzer, 2000). Complementary to this, the grasshopper eye lobe also lacks ventrally restricted expression of fng while its expression in and anterior to the furrow is conserved (Dong and Friedrich, unpublished; Dearden and Akam, 2000). These results suggest the absence of an N signaling based equatorial organizing center in the grasshopper retina. Although surprising at first glance, this is consistent with the lack of evidence for planar cell polarity patterning in the grasshopper retina (Wilson et al., 1978). Furthermore, while the N pathway is an essential upstream growth activator in the Drosophila eye disc, many additional signaling factors stimulate proliferation in the Drosophila eye disc such as Dpp, Egfr and Wg (Burke and Basler, 1996; Halfar et al., 2001; Lee and Treisman, 2001). It is therefore conceivable that different signaling pathways support retina growth in grasshopper without participation of N. To determine if the N signaling based dorsoventral compartment formation is a derived aspect of Drosophila eye imaginal disc development it will be necessary to analyze the relevant genes in other insect species with dorsoventral specific pattern elements. Shared genetic mechanisms would indicate the function of an evolutionarily conserved patterning mechanism that was lost during the evolution leading to grasshopper. Lack of dorsoventral compartment specific expression of wg and fng on the other hand would suggest that dorsoventral patterning mechanisms evolved multiple times independently.
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While the mechanisms related to dorsoventral patterning are suspect of evolutionary change, establishment of the anterior posterior axis in the Drosophila eye disc is likely to follow ancient paths. The primary determinant of the anteroposterior axis is the expression of wg, which changes from dorsal specific expression in the second larval instar to a pair of dorsal and ventral domains at the anterior margin of the eye field with beginning of the third instar (Fig. 4). As Wg inhibits furrow initiation, movement and neuronal differentiation, the initiation of retina differentiation is forced to occur at maximal distance to these expression domains at the midline of the posterior eye lobe margin (Ma and Moses, 1995
; Treisman and Rubin, 1995). Furthermore, ectopic activation of Wg signaling can enforce anterior compartment identity to the posterior of the retinal eye field (Lee and Treisman, 2001). Polar expression of wg in front of the retina field consistent with this patterning function was found conserved in several arthropod species ranging from Schistocerca and Tribolium to crustacean and myriapod species (Friedrich and Benzer, 2000; Niwa et al., 2000; Duman-Scheel et al., 2002; Hughes and Kaufman, 2002). |
INITIATION OF DIFFERENTIATION: WITH OR WITHOUT DPP? |
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The initiation of retina differentiation in the Drosophila eye disc has been genetically dissected into two discrete phases (Kumar and Moses, 2001b
). Phase one or "furrow birth," which involves the primordial activation of morphogenetic furrow formation and photoreceptor differentiation at the posterior eye disc margin, requires activity of the N, EgfR and Hh signaling pathways (Dominguez and Hafen, 1997; Borod and Heberlein, 1998; Kumar and Moses, 2001b). The second phase begins with the continuous initiation of differentiation along the disc margins necessary for lateral increase of the eye field size. This process, dubbed "reincarnation," depends on input from the Egfr and Dpp signaling pathways (Chanut and Heberlein, 1997; Kumar et al., 1998; Curtiss and Mlodzik, 2000). In the grasshopper eye lobe, furrow initiation occurs also at the posterior margin centered at the midline followed by anterior progression of the furrow and lateral extension of the eye field (Fig. 2C). Considering the conserved spatial dynamics of retina differentiation it seems likely that the same regulatory mechanisms are at work in the grasshopper eye. However, comparative expression pattern analyses of the key player dpp indicate partial evolutionary divergence at the molecular regulatory level. In Drosophila, dpp is strongly expressed along the posterior and lateral disc margins before furrow birth and continues to be expressed along the lateral eye disc margins during furrow reincarnation (Blackman et al., 1991; Cho et al., 2000). This is consistent with functional evidence for Dpp involvement in furrow initiation (Blackman et al., 1991; Chanut and Heberlein, 1997; Pignoni and Zipursky, 1997). In situ hybridization experiments in Schistocerca failed to detect expression of dpp in the posterior and lateral grasshopper eye lobe ectoderm margins prior to and following furrow initiation, which argues against a role of dpp in both phases of grasshopper furrow initiation (Friedrich and Benzer, 2000).
It has been proposed that the underlying cause for this discrepancy between grasshopper and Drosophila eye development may be the divergence of mechanisms that control the expression of wg in the eye field (Friedrich and Benzer, 2000). In Drosophila, dpp is essential for transforming the dorsal compartment specific expression of wg into the anterior polar domains. The dorsal expression domain of the morphogenetic furrow inhibitor wg extends initially to the posterior margin of the disc during the dorsoventral compartment patterning phase (Fig. 4A) (Cho et al., 2000). During the late second larval instar, wg becomes repressed at the posterior margin by dpp. In the third instar eye disc, dpp continues to be required for repression of wg transcription in both the dorsal and ventral margin (Royet and Finkelstein, 1997; Cho et al., 2000). A similar wg expression pattern change is not observed during grasshopper eye lobe development where wg is expressed in anterior polar domains from very early on (Friedrich and Benzer, 2000). The wg and dpp expression patterns described in the developing Tribolium eye lobes match that in the Schistocerca eye lobes (Nagy and Carroll, 1994; Sanchez-Salazar et al., 1996). The lack of dpp expression in the grasshopper eye lobes prior to the initiation of the morphogenetic furrow thus correlates with a fundamental difference regarding the emergence of the conserved expression of wg in the anterior eye field of primitive insects. It is therefore possible that the requirement of dpp for furrow initiation along the lateral margins of the Drosophila eye disc evolved in conjunction with its apparently derived role of suppressing wg from these regions.
Recent studies however demonstrated that dpp promotes morphogenetic furrow initiation by activating the expression of retina determination genes such as eya (Curtiss and Mlodzik, 2000). Provided the respective Dpp signal is not secreted by extraretinal tissues in the grasshopper (see below), or replaced by related TGF-ß related signal transduction pathways, the differences between the regulatory networks controlling furrow initiation in Drosophila and Schistocerca might even be deeper.
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PROGRESSION OF DIFFERENTIATION |
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Once initiated, the furrow moves from posterior to anterior laying out the regular array of developing ommatidial precursor clusters in the posterior eye field. In Drosophila, the progression of this dynamic differentiation border is maintained by the combined action of at least three signal transduction pathways, which coordinate the transcriptional control of retina differentiation (Bessa et al., 2002
) (Fig. 5). The transcription factors Hth, Tsh and Ey, which are coexpressed in the anterior disc region, have been proposed to interact physically and keep the anterior eye disc tissue in an undifferentiated growth state (Bessa et al., 2002). The long-range signaling factor Dpp, expressed in the furrow, instructs cells far anterior to the furrow to advance from this state into a preproneural state (PPN), which is characterized by repression of retina differentiation antagonist hth and expression of the proneural transcription factor daughterless (da). Precocious neural differentiation in the PPN zone is prevented by the helix-loop-helix transcription factor hairy (h), which is also activated by dpp. Exit from the PPN state is induced via activation of the N signaling pathway by the short-range factor Dl, which is also expressed in the furrow. This leads to repression of the neuronal specification antagonists extramachrochaete (emc) and h, allowing for expression of ato in the furrow. The initial uniform expression of ato in the furrow refines to R8 photoreceptor cells posterior to the furrow. This is followed by rapid recruitment of additional photoreceptors cells to the newly emerging ommatidia. The positive feedback loop between differentiation and induction of furrow progression is closed by the expression of Hh in the maturing photoreceptor cells, which diffuses anteriorly and activates N and dpp transcription in the furrow.
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As the basic cellular morphology of the morphogenetic furrow is conserved in diverse arthropods there is little reason to suspect evolutionary divergence of the regulatory network driving furrow progression. This is furthermore suggested by the strikingly similar involvement of hh and ato in vertebrate eye development indicating evolutionary conservation at a deep phylogenetic level (Neumann and Nuesslein-Volhard, 2000
; Brown et al., 2001). Nonetheless, comparative expression analysis in the developing retina of Schistocerca and Tribolium suggests partial evolutionary diversification (Fig. 5). In Drosophila dpp begins to clear from the posterior margin and to increase expression in the morphogenetic furrow after furrow initiation (Blackman et al., 1991). In Schistocerca dpp is expressed at low levels throughout the anterior eye field ectoderm in addition to an expression domain posterior to the furrow, which is associated with the area of the eye lobe retina where the photoreceptor axons project from the retina into the lamina (Friedrich and Benzer, 2000). This finding has implications regarding possible mechanisms involved in grasshopper furrow progression by comparison to Drosophila. Grasshopper dpp may either instruct the entire anterior retina field to enter the PPN state or carry out an entirely different function. Ongoing studies in our lab show that the homeodomain transcription factor exd, the essential dimerization partner of hth, is expressed neither in the grasshopper eye nor in regions immediately adjacent to it. This implies the absence of hth mediated transcriptional control in the anterior of the grasshopper eye lobe (Dong and Friedrich, unpublished). The lack of a Drosophila PPN related transcriptional switch of hth expression in the grasshopper eye field points to the possibility that the furrow progression promoting function of dpp is not conserved. Interestingly, Drosophila dpp is not essential for furrow progression as hh on its own can induce the PPN state although at a slower pace (Burke and Basler, 1996; Greenwood and Struhl, 1999). It has been proposed that the expression of dpp in the Drosophila morphogenetic furrow evolved to accelerate furrow progression in this fast developing species (Friedrich and Benzer, 2000; Bessa et al., 2002). This idea was based on the assumption of an otherwise largely conserved network of transcriptional control of retina differentiation. The correlated lack of hth/exd in the grasshopper eye lobe however raises the possibility that the divergence of dpp expression is connected to more fundamental differences in the early control of retina differentiation. This may be related to the evolutionarily derived dynamic determination of head versus retina fate in the Drosophila eye disc. |
RETINAL FATE COMMITMENT (II): EYE VERSUS HEAD CUTICLE |
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Coexpression of the seven essential eye specification master genes during the second larval instar poises cells in the Drosophila eye disc to adopt retinal fate (Kumar and Moses, 2001a
). However, only approximately two thirds of the posterior disc will differentiate into retina while cells in the anterior margin give rise to adjacent head cuticle elements (Haynie and Bryant, 1986). Consistent with this, the domain of eye specification transcription factor coexpression is centered in the posterior of the eye disc and does not extend through the anterior disc (Bessa et al., 2002). At the time of furrow progression, for instance, the expression of dac and eya does not extend more anteriorly than to the anterior border of the PPN zone due to hth mediated repression. The expression domain of hth on the other hand which initially covers the entire early eye-antennal imaginal disc becomes progressively restricted to the posterior eye disc due to repression by Dpp emanating from the moving furrow (Pichaud and Casares, 2000; Bessa et al., 2002). There are thus two commitment stages through which cells of the eye disc pass. During the second larval instar cells become committed to participating in retina over antenna associated head compartment formation. During the third larval instar, cells adopt retina fate if they fall within the reach of the morphogenetic furrow while developing into head cuticle components otherwise. At this stage, retina fate is promoted in the posterior disc by the combined action of the dpp, hh, N and Egfr signaling pathways. The specification of head cuticle fate is in the realm of the anterior polar expression domains of wg, which besides activating hth expression in the anterior eye disc field, is a negative regulator of photoreceptor differentiation itself (Ma and Moses, 1995; Treisman and Rubin, 1995; Pichaud and Casares, 2000). In addition, there is evidence that Wg signaling can induce head cuticle morphogenesis as opposed to retina differentiation (Royet and Finkelstein, 1997; Baonza and Freeman, 2002). In summary, wg is not only essential for determining the anterior border to the progression furrow but also for the morphogenesis of major parts of the dorsal (vertex) and ventral (gena) Drosophila head. Consistent with this, the respective eye disc anlagen reside within the expression domains of hth and wg (Pichaud and Casares, 2000).
Although the expression of wg in two polar domains anterior to the developing retina is highly conserved, the fate map of wg expressing cells in the developing grasshopper head shows significant differences with that in the Drosophila eye disc (Fig. 6). Already the early lateral wg expression domains reside within the anterior eye field of the eye lobe but do not extend into areas outside the eye lobes. The discrepancy is most obvious with regards to the dorsal head regions, which give rise to the lateral and median ocelli. These lie within the wg expression domains in Drosophila but are remote from the wg expression domains in the grasshopper eye lobe. Further support for evolutionary divergence of wg related patterning of the adult Drosophila head is indicated by the lack of Wg signaling downstream target gene expression in the grasshopper head. The transcription factor engrailed, which is activated by wg via otd, is required for ocelli formation in Drosophila but not expressed in the differentiating ocelli of the grasshopper embryo (unpublished observation) (Royet and Finkelstein, 1995). The expression of wg in the grasshopper eye lobe is thus compatible with a role in negatively regulating furrow progression and thereby organizing the anterior border of the retina, but not with patterning adjacent head cuticle regions to the extent it is occurring in Drosophila. This difference in wg patterning functions correlates with the fact that partitioning of head versus retina field by formation of the eye lobes has been completed before furrow initiation during grasshopper embryonic head development. The integration of retina differentiation and adult head cuticle partitioning under antagonistic control by wg and dpp represents a derived aspect of Drosophila eye disc development.
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CONTROL AT A DISTANCE (I): EXTRARETINAL SIGNALING SOURCES |
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The antagonism of anterior head cuticle versus retina differentiation is only one example for the coordination of retina differentiation with adult head development in the Drosophila eye-antennal imaginal disc. To embrace the entire scope of this patterning aspect, it is important to recall the double layer nature of the sac-like eye-antennal imaginal disc. The apical surface of the disc proper, the posterior compartment of which forms the retina, is overlaid by the peripodial membrane, which contributes a considerable part of the posterior dorsal head cuticle (Haynie and Bryant, 1986
). There is thus not only a need to coordinate growth and differentiation between the anterior and posterior pole of the disc proper but also between the peripodial membrane and the disc proper. Recent studies have provided evidence of regulatory communication between these tissue layers by exchange of signaling factors across the lumen of the disc. Hh, Dpp and Wg for instance are expressed in the peripodial membrane of the early eye-antennal disc from where they instruct dorsoventral compartment formation in the disc proper (Cho et al., 2000). Similarly, Fng and Ser have been reported to be expressed in the peripodial membrane instead of the disc proper in the context of dorsoventral compartment formation (Gibson and Schubiger, 2000). Information exchange seems to proceed in both directions as Dpp expressed in the disc proper furrow has been reported to maintain cell survival in the peripodial membrane (Gibson et al., 2002). Although results from these studies differ in some detail, Ser for instance has also been described as disc proper located target of thh signaling (Cho et al., 2000), the evidence for signal exchange between disc proper and peripodial membrane is overall consistent and compelling. Active and passive transport mechanisms have been proposed to be involved in the exchange of signaling molecules between the two tissues. Dpp, expressed in the furrow of the disc proper has been found to accumulate in the disc lumen (Gibson et al., 2002). Cellular processes reaching from the peripodial membrane to the disc proper have been proposed to transport Hh, Wg and Dpp protein (Cho et al., 2000; Gibson and Schubiger, 2000).
From an evolutionary perspective, the regulatory interactions between peripodial membrane and disc proper represent a derived patterning aspect of the Drosophila eye-antennal disc. In the more primitive Tribolium eye placode no peripodial membrane is formed and the differentiating retina cells contact the cuticle of the larval head (Friedrich et al., 1996). There is thus no candidate non-retinal signaling source facing the Tribolium eye placode. Likewise, no peripodial membrane equivalent tissue exists in the developing grasshopper embryonic head. Nonetheless, extraembryonic tissues of the grasshopper embryo could serve as analogous extraretinal patterning sources. From gastrulation to about 35% of development, the amnionic membrane covers most of the grasshopper embryo reaching from the dorsal margins ventrally. The eye lobe ectoderm in particular develops in contact with the amnionic membrane (Friedrich and Benzer, 2000). Interestingly, dpp is expressed in the dorsal edges of the grasshopper amnionic membrane from where it could diffuse to the eye lobes (personal observation). The amnionic membrane will therefore have to be considered as potential signaling source in future analyses of eye development in the grasshopper and non-holometabolous insects in general.
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CONTROL AT A DISTANCE (II): HORMONAL REGULATION OF RETINA DIFFERENTIATION |
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In addition to local signals hormonal instructions affect the progression of the Drosophila morphogenetic furrow from a distance. During postembryogenesis, ecdysone is secreted from the larval ring glands and metabolized into the hormone 20-hydroxyecdysone (20E) in peripheral tissues. Each of the three larval molts in Drosophila is associated with a transient peak in 20E concentration, which instructs the epidermal cells to secrete new cuticle. These 20 levels peaks occur in the presence of a second hormonal mediator, juvenil hormone (JH), which preserves the growth character of the molts. JH levels drop during the last larval instar and a moderate ecdysone peak induces the larva to stop food uptake and to prepare for pupation. This stage is the wandering stage during which retina differentiation is initiated. The next ecdysone peak, which induces the pupal molt, is accompagnied by rising JH levels. Juvenil hormone levels drop in the early pupa. A final pupal 20E level peak in the absence of JH initiates the terminal differentiation of adult structures including the retina (for review see Riddiford, 1993
). Molecular genetic analyses have revealed that the progression of the morphogenetic furrow and the early differentiation of photoreceptor clusters are sensitive to 20E levels as well as to the presence of components of the ecdysteroid signal transduction machinery. Conditional genetic ecdysteroid depletion in D. melanogaster causes stall of furrow progression, incorrect initiation of R8 founder cells, and loss of neuronal differentiation (Brennan et al., 1998). Somewhat conflicting results have been obtained by in vitro culturing studies in which morphogenetic furrow progression and photoreceptor differentiation could be observed in the absence of ecdysteroid supplements (Li and Meinertzhagen, 1997). Nonetheless, the involvement of ecdysteroid signaling in the control of furrow progression has been further substantiated by the finding that the furrow also stalls in tissue mutant for the ecdysteroid signaling immediate early gene Broad complex (BR-C) isoform Z2 (Brennan et al., 2001). The canonical ecdysteroid receptor complex consisting of the ecdysteroid receptor (EcR) and the RXR homolog Ultraspiracle (Usp) seems not to be involved in the transduction of the signal as the furrow is not affected in EcR mutant tissue (Brennan et al., 2001). Loss of Usp however causes acceleration of furrow progression associated with ectopic expression of the BR-C isoform protein Z1 anterior to the furrow. The discrepancy compared to the ecdysteroid depletion phenotype is explained by the fact that Usp acts as repressor when unbound, but as transcriptional activator in the ligand bound situation (Zelhof et al., 1997; Ghbeish and McKeown, 2002). The biological significance of the hormonal control of early retina differentiation in Drosophila remains to be determined. One possibility is that the hormonal clues are necessary to align the multitude of organ differentiation events with each other and the organism's growth progress. The need for hormonal regulation of early retina differentiation is obvious for a second holometabolous species, in which the effect of ecdysteroid levels on retina development has been carefully investigated, the tobacco hornmoth Manduca sexta (Champlin and Truman, 1998). It is the transient halt of development during pupal diapause in Manduca, which is controlled by the reversible block of early retina development at below threshold ecdysteroid levels. This responsiveness of the Manduca retina changes during the final pupal ecdysteroid surge, which irreversibly terminates the progression of the morphogenetic furrow and triggers terminal differentation throughout the retina field in a concerted manner. The final pupal ecdysteroid peak has the same consequences in Manduca and Drosophila including rhabdomere formation, pigment synthesis and lens cuticle secretion from cone cells. In both systems, these developmental responses can be triggered in cultured retinas by application of 20E (Li and Meinertzhagen, 1995; Champlin and Truman, 1998). In combination, these data suggest that the ecdysone dependence of terminal retina differentiation is an ancestral aspect of postembryonic eye development in holometabolous insects. The regulatory effect of ecdysteroid signaling on early retina differentiation may also trace back to the origin of holometabolous insects but obviously experienced lineage specific modifications.
The shared ecdysteroid signaling dependence of postembryonic retina differentiation in Manduca and Drosophila raises the question if the hormonal control of eye development evolved in the ancestral lineage of holometabolous insects, or was inherited from hormonal mechanisms already involved in the control of retina differentiation in primitive insects. Ecdysteroid level peaks have long been known to induce molting both during embryogenesis and postembryogenesis in hemimetabolous insects including orthopterans such as Schistocerca (Lagueux et al., 1979). Less information existed regarding possible involvement in additional differentiation processes. Cell proliferation at the postembryonic morphogenetic furrow in Schistocerca has been reported to reach highest levels between molts while being silent during molting, which is induced by ecdysteroid level peaks (Anderson, 1978). These data suggest that ecdysteroids may have an inhibiting effect on furrow progression during grasshopper postembryogenesis. In culturing experiments of embryonic Schistocerca eye lobes, however, supplementing 20E stimulated cell proliferation and the rate of morphogenetic furrow progression (Dong et al., 2003). Also aspects of terminal differentiation such as screening pigment synthesis were significantly enhanced by 20E application. At the same time, base levels of furrow progression, cell proliferation and screening pigment synthesis could be observed in culture even when ecdysteroid signaling was blocked by application of ecdysteroid antagonist Cucurbitacin B suggesting that ecdysteroid signaling is not essential for retina differentiation in Schistocerca (Dong et al., 2003). In combination, the available data from Schistocerca indicate that retinal development is not dependent on but sensitive to ecdysteroid levels both during embryogenesis and postembryogenesis in primitive insects. The stringent control of early retina differentiation in species such as Manduca may have evolved by modification of preexisting mechanisms of hormonal control. These mechanisms may already have been related to the developmental control of diapause, which is also observed in primitive insects (Tawfik et al., 2002). The critical dependence of terminal differentiation on elevated ecdysteroid levels during pupation on the other hand has to be added to the list of derived aspects of Drosophila eye development when compared to primitive insects.
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SUMMARY AND PERSPECTIVES |
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Given the infancy of molecular genetic studies of eye development in non-Drosophila insects our understanding of insect eye development evolution is by necessity still incomplete and preliminary. Nonetheless, the data accumulated so far seem to build a strong case for the hypothesis that relatively recent evolutionary modifications affected many steps of the molecular developmental control of Drosophila retina formation. Some generalization may be helpful to structure the diversity of observations presented. The evolution of rapid embryogenesis in higher flies via an extreme form of long germband development affected the early patterning of the embryonic visual primordium. The restriction of retina differentiation to late stages of postembryonic development, which separates holometabolous insects from primitive hemi- and ametabolous insects, involved changes in the timing, and perhaps logic, of retina primordium determination, and modifications of the hormonal control of retina development. The evolution of postembryonic adult head primordium formation from internalized imaginal discs, which allowed the emergence of the acephalic larva typical for brachyceran flies, is likely to have enforced the widest range of developmental modifications. These may concern the control of initiation and progression of retina differentiation, the developmental communication between retina and non-retina tissues, and the dynamic partitioning of retina versus adjacent head cuticle compartments. A comprehensive analysis of eye development in Schistocerca and Tribolium holds promise of elucidating the apparently highly eventful evolutionary history of Drosophila visual system development. In addition, it will be necessary to extend the comparison to crustaceans to verify the ancestral status of processes operating in primitive insects by outgroup comparison (Hafner and Tokarski, 1998
; Melzer et al., 2000; Harzsch and Walossek, 2001).
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ACKNOWLEDGMENTS |
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I am grateful to the members of the lab for reading the manuscript and three anonymous reviewers for helpful comments. This research was funded by NSF grants DBI-0070099 and DBI-0091926.
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FOOTNOTES |
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1 From the Symposium Comparative and Integrative Vision Research presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8 January 2003, at Toronto, Canada.
2 E-mail: mf{at}biology.biosci.wayne.edu
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