Molecular characterization and embryonic origin of the eyes in the common house spider Parasteatoda tepidariorum
- Christoph Schomburg1,
- Natascha Turetzek1,
- Magdalena Ines Schacht1,
- Julia Schneider1,
- Phillipp Kirfel1, 2,
- Nikola-Michael Prpic†1 and
- Nico Posnien†1Email author
© Schomburg et al.; licensee BioMed Central. 2015
Received: 13 February 2015
Accepted: 10 April 2015
Published: 28 April 2015
Two visual systems are present in most arthropod groups: median and lateral eyes. Most of our current knowledge about the developmental and molecular mechanisms involved in eye formation in arthropods comes from research in the model system Drosophila melanogaster. Here, a core set of retinal determination genes, namely, sine-oculis (so), eyes absent (eya), dachshund (dac), and the two pax6 orthologues eyeless (ey) and twin of eyeless (toy) govern early retinal development. By contrast, not much is known about the development of the up-to-eight eyes present in spiders. Therefore, we analyzed the embryonic expression of core retinal determination genes in the common house spider Parasteatoda tepidariorum.
We show that the anlagen of the median and lateral eyes in P. tepidariorum originate from different regions of the non-neurogenic ectoderm in the embryonic head. The median eyes are specified as two individual anlagen in an anterior median position in the developing head and subsequently move to their final position following extensive morphogenetic movements of the non-neurogenic ectoderm. The lateral eyes develop from a more lateral position. Intriguingly, they are specified as a unique field of cells that splits into the three individual lateral eyes during late embryonic development. Using gene expression analyses, we identified a unique combination of determination gene expression in the anlagen of the lateral and median eyes, respectively.
This study of retinal determination genes in the common house spider P. tepidariorum represents the first comprehensive analysis of the well-known retinal determination genes in arthropods outside insects. The development of the individual lateral eyes via the subdivision of one single eye primordium might be the vestige of a larger composite eye anlage, and thus supports the notion that the composite eye is the plesiomorphic state of the lateral eyes in arthropods. The molecular distinction of the two visual systems is similar to the one described for compound eyes and ocelli in Drosophila, suggesting that a unique core determination network for median and lateral eyes, respectively, might have been in place already in the last common ancestor of spiders and insects.
KeywordsEye development Spiders Retinal determination genes Parasteatoda tepidariorum
The most comprehensive understanding of the processes involved in adult eye formation is available for insects, mainly from work performed in the fruit fly Drosophila melanogaster. There, the lateral compound eyes and the dorsal-median ocelli (Figure 1) originate from a few cells of the visual anlage in the dorsal head neuroectoderm in the embryo [8-10]. During the first larval instar, these cells are part of the eye-antennal imaginal disc that undergoes massive proliferation throughout larval and pupal development . Within the eye-antennal imaginal disc, the two visual systems are determined in non-overlapping domains, implying that the anlagen of both visual systems develop largely independent of one another [12,13].
The retinal field (that is, the anlage of the lateral compound eyes) of the eye-antennal imaginal disc is determined on a molecular level by the action of a cascade of transcription factors that is known as the retinal determination gene network (RDGN). In summary, the pax6 genes eyeless (ey) and twin of eyeless (toy) activate an auto-regulatory network of transcription factors involving sine-oculis (so), eyes absent (eya), and dachshund (dac) . The Drosophila ortholog of the six3 gene, optix, is involved in eye morphogenesis in an ey-independent manner  and has been linked to differentiation processes within the retinal field . The core of the RDGN not only determines the retinal field that gives rise to the lateral compound eyes but also operates in the dorsal-median ocelli . However, initial establishment of the ocellar primordium requires unique regulatory interactions between engrailed (en), hedgehog (hh), and orthodenticle (otd), which eventually lead to RDGN activation via eya in the ocelli anlagen [12,17-19]. Additionally, the RDGN genes ey and dac are only present in the determination of the lateral compound eyes [6,7,20]. These data suggest that the molecular mechanisms underlying the determination of the lateral and median eyes represent a combination of shared and unique aspects.
Intriguingly, comparative expression data accumulated over the last decades suggest that the core RDGN known from Drosophila might be conserved in the various different bilaterian eye types [3,21]. For instance, members of the pax family genes are the most widely conserved eye selector genes and appear to initiate eye development in all animals. pax6 orthologues are expressed during eye development, for example, in Cnidarians [22-25], the lancelet Branchiostoma floridae , the polychaete Platynereis dumerilii , the ascidian Phallusia mammillata , and the onychophoran Euperipatoides kanangrensis . However, more detailed examination of expression and/or function of RDGN genes also revealed functional differences. For instance, in the flour beetle Tribolium and in Drosophila, the pax6 orthologues ey and toy seem to play a more dominant role during larval eye development, rather than in the adult eyes . Similarly, in the American Horseshoe Crab, Limulus polyphemus, pax6 does not seem to be expressed in the eye primordia during late embryogenesis, implying that it might not be involved in retinal determination .
The arthropod ground plan includes both median and lateral eyes as two separate visual systems. However, in extant arthropod groups, one of the two systems is usually the dominant visual system, strongly suggesting that a single visual system is largely sufficient. For instance, in insects, the main visual organs are the lateral eyes (compound eyes), whereas the median eyes are simple lens eyes (ocelli) with only poor visual capacities. The ocelli have instead acquired novel functions, for example, in flight stability control , or have been entirely reduced in many insect groups . In contrast, in most spiders, the median eyes represent the main visual system, while the lateral eyes mostly visualize movement . Insects and spiders have thus used different evolutionary strategies for their visual systems.
However, so far only little is known about eye development in spiders and the molecular genetic mechanisms that govern their formation. Therefore, we have isolated homologues of several retinal determination genes known from Drosophila in the spider Parasteatoda tepidariorum and present here an analysis of their expression patterns throughout head development. P. tepidariorum represents an excellent model system for comparative studies due to its short life cycle, access to offspring throughout the year, and various established methods like in situ hybridization and RNA interference . We show that the anlagen of the median eyes originate from an anterior median position in the developing head, while the lateral eyes develop from a more lateral position. Intriguingly, the lateral eyes develop from a single field of cells that splits into the three individual lateral eyes during late embryonic development. Besides differences in the embryonic origin, we identified a unique combination of determination gene expression in the anlagen of the lateral and median eyes, respectively. This molecular distinction of the two visual systems is similar to the one described for compound eyes and ocelli in Drosophila, suggesting that a unique core determination network for median and lateral eyes, respectively, might have been in place already in the last common ancestor of spiders and insects.
Animal culture and gene cloning
Embryos were obtained from our laboratory stock in Göttingen. The embryos were staged as previously published . The following already published eye determination genes were used in this study: pax6.1 (FM945394.1), dac1 (FM945397.1), six3.1 (AB605265.1), six3.2 (AB605266.1), and otd1 (AB096074.1). The sequences of additional genes were identified by BLAST search of the sequences from D. melanogaster against the P. tepidariorum transcriptome : pax6.2 (KP725068), so1 (KP725069), so2 (KP725070), eya (KP725071), dac2 (KP725072), otd2 (KP725073), and peropsin (KP725074). Paralogs were named “1” and “2,” respectively, according to their sequence similarity to the D. melanogaster sequence. Total RNA was extracted from a mix of all embryonic stages using TRIzol® (Life Technologies, Carlsbad, CA, USA). cDNA was synthesized from total RNA with the SMARTer™ PCR cDNA Synthesis Kit (Clontech, Mountain View, CA, USA). Gene-specific cDNA fragments were amplified with primers designed with Primer3  (Additional file 1: Table S1) and cloned into the pCR®II vector using the TA Cloning® Kit Dual Promoter (Invitrogen, Life Technologies, Carlsbad, CA, USA).
Pylogenetic analysis of spider Opsin homologues
For phylogenetic analysis of Opsin homologues, candidate sequences were identified by BLAST search of the D. melanogaster Rhodopsin protein sequences against the transcriptome of P. tepidariorum . In addition to P. tepidariorum sequences, Opsin protein sequences for a multiple sequence alignment were obtained from published sources [43-46] (see also Additional file 2: Table S2). Multiple sequence alignment was performed with MUSCLE version 3.8.31 [47,48]. The pylogenetic tree was inferred using the parallel version of MrBayes 3.2.4 [49-52] with default settings for the likelihood model and the priors for the phylogenetic model. The amino-acid substitution model was set to “Blosum” that was determined as the model best suited for the input data by the MrBayes program.
In situ staining and imaging
In situ hybridization and nuclear staining with SYTOX® Green were performed as described before [53,54] with minor modifications. Instead of PBST, we used MABT for rehydration and washing steps after the hybridization, as well as commercially available blocking agent from Roche (Basel, Switzerland) (2% in MABT). Images were taken with Leica M205 FA binocular (Leica Microsystems, Wetzlar, Germany) equipped with a QImaging MicroPublisher 5.0 RTV camera (QImaging, Surrey, Canada) and UV light. Stacks of nuclear SYTOX® stainings were taken with a Zeiss LSM 510 microscope (Zeiss, Oberkochen, Germany). Images were corrected for color values and brightness with Adobe Photoshop image processing software (version 12.0).
Morphogenesis of the non-neurogenic ectoderm in the embryonic head
P. tepidariorum has one pair of median eyes and three pairs of lateral eyes (Figure 1A). Similar to several other members of the spider family Theridiidae, the anterior (ALE) and posterior lateral eyes (PLE) are located very close to each other , and in P. tepidariorum adults, they even share a common socket in the carapace (Figure 1A).
Pt-peropsin is expressed in all eye primordia at late embryonic stages
Since the eye primordia in P. tepidariorum are morphologically visible only late during embryonic and postembryonic development, we sought to identify a molecular marker that prefigures the eye primordia. We identified one homologue of the peropsin group and four homologues from the group of r-Opsins (Additional file 3: Figure S1). We cloned these five opsins and analyzed their expression throughout late embryonic development (Figure 3B and not shown). Pt-peropsin is the only opsin homologue that is detectable at embryonic stages. It is expressed at stage 14 in three spots on either side of the prosomal shield (Figure 3B, white arrowheads). These expression domains coincide morphologically with the indentations of the lateral eyes in the epidermal tissue (Figure 3A, black arrowheads). Additionally, Pt-peropsin is expressed in two spots in the anterior median region of the prosomal shield (Figure 3B, black arrowheads). In this median position, the two median eyes will develop during first instar stages . In summary, we identify Pt-peropsin as embryonic molecular marker for developing eyes in the spider P. tepidariorum.
Spider homologues of Drosophila retinal determination genes
We have isolated homologues of key components of the retinal determination gene network known from Drosophila, and have studied their expression in all eye primordia of P. tepidariorum. In the following, we give a detailed account of the expression of all studied genes during the developmental stages 10 to 14, which comprise the time span between the formation of the non-neurogenic ectoderm at the anterior and lateral rim of the head lobes, the overgrowth of the brain anlage, and the development of the primordia of the lateral and median eyes within the non-neurogenic ectoderm.
Homologues of pax6
Pt-pax6.2 is expressed in a transversal stripe across the neurogenic ectoderm in the head lobes and a smaller domain, which surrounds the lateral furrow (Figure 4F, arrowhead). At stages 11 and 12, the transversal domain condenses, while the expression surrounding the lateral furrow ceases (Figure 4G,H). During non-neurogenic ectoderm overgrowth at stages 13 and 14, Pt-pax6.2 shows a diffuse expression in the underlying brain anlagen (Figure 4I,J). Note that the non-neurogenic ectoderm outside of the anterior and lateral furrows is free of Pt-pax6.1 and Pt-pax6.2 expression throughout the embryonic stages analyzed.
Homologues of six1/sine-oculis
Pt-so2 is expressed in the labrum at stage 10 (Figure 5F), but is not expressed in the brain anlage or the non-neurogenic ectoderm during stages 10 to 12 (Figure 5F to H). However, once the brain anlage is fully overgrown by the non-neurogenic ectoderm, a new expression domain of Pt-so2 arises at stage 13 in the non-neurogenic ectoderm close to the posterior-lateral edge of the head lobes (Figure 5I, arrowhead) and persists throughout stage 14 in the primordia of the anterior lateral eyes (Figure 5J, arrowhead).
Homologue of eyes-absent
Homologues of dachshund
Pt-dac2 is not expressed in the head lobes before stage 12 (Figure 8F,G). At stage 12, expression of Pt-dac2 appears anterior to the labrum and in two distinct domains in the lateral head (Figure 8H). During stages 13 and 14, all primordia of the lateral eyes express Pt-dac2 very strongly (white arrowheads in Figure 8I,J).
Homologues of six3/optix
Homologues of orthodenticle
At stages 10 and 11, Pt-otd2 is expressed in a broad domain in the center of the developing brain and in two connected domains at the rim of the head lobes (white arrowheads in Figure 11F,G). This entire expression is very dynamic during further development and finally covers most of the forming brain (Figure 11H to J). Parts of the anterior rim domain move posteriorly with the overgrowing non-neurogenic ectoderm during stages 12 to 14 (white arrowheads in Figure 11G to J), resulting in Pt-otd2 expression in two small clusters of cells in the anterior-median non-neurogenic ectoderm that correspond to the median eye primordia (white arrowheads in Figure 11J).
Embryonic origin of median and lateral eyes
Although the eyes become morphologically visible only in late embryonic stages (in the case of the lateral eyes) or even in postembryonic stages (in the case of the median eyes) , the primordia of all eyes can be identified much earlier based on their expression of conserved retinal determination genes.
The primordia of the median eyes are defined in non-neurogenic tissue that is at first located at the anterior rim of the head lobes, but then moves with the leading edge of the overgrowing tissue and finally the median eyes are situated at the anterior rim of the developing carapace. This movement of the median eye primordia can be followed best using the expression of Pt-so1 because this gene is expressed in the median eye primordia from their initial allocation at the anterior rim of the head lobe until their final location at the anterior rim of the carapace (Figure 6).
The lateral eye primordia are also formed in non-neurogenic ectoderm, but at the lateral rim of the head lobes and they do not move with the leading edge of the overgrowing non-neural ectoderm. Intriguingly, our data suggest that at a molecular level all lateral eyes are initially specified as a single field of cells on each side of the head lobes. Differentiation into three separate lateral eyes then occurs later by splitting of the original uniform eye field. The first splitting gives rise to the median lateral eyes and the primordium of the posterior and anterior lateral eyes. In a second splitting event, the latter primordium then separates into the posterior and the anterior lateral eyes. It is tempting to speculate whether this composite lateral eye primordium is a remnant of a phylogenetically older complex lateral eye primordium [5,60]. Indeed, basal chelicerates (for example, L. polyphemus) have complex lateral eyes , several fossil arthropod groups have complex lateral eyes (for example, Trilobites) , and multi-facetted complex eyes are widespread in the crustaceans and insects . This suggests that the formation of the lateral eyes via a common eye field that is subsequently subdivided into smaller eye units represents the plesiomorphic condition of the lateral visual system in the arthropods.
Every eye type expresses a unique combination of transcription factors
In summary, we find hints that a separation of the core eye determination network into two separate functional units governing median and lateral eye formation, respectively, might have been present already in the ancestral arthropod and thus may predate the split between chelicerates and insects. While in insects and spiders, the anlagen of median eyes are defined by the presence otd and a lack of So/Eya-mediated dac activation, lateral eye development relies on the action of Dac and Six3 in addition to the So/Eya complex that is necessary for the formation of all eyes (Figure 12A,B). Additional molecular diversification of lateral eyes in spiders might be facilitated by the presence of paralogous eye determination genes.
The role of Pax6 during spider eye development
Intriguingly, we do not detect late expression of the two pax6 orthologues in any of the eye primordia of P. tepidariorum. A similar observation has been made in the American Horseshoe Crab L. polyphemus where late embryonic eye anlagen are free of pax6 expression . This result is unexpected since Pax6 is required for eye development not only in insects but also, for example, in mammals [68-70]. In Limulus, early pax6 expression was not studied but qPCR results imply an activity prior to the analyzed late stages . Hence, it is likely that Pax6 is required early during anterior development to specify the future eye anlagen. This hypothesis is supported by Pt-pax6.1 expression at the anterior rim of stage 6/7 germ disc embryos of P. tepidariorum (not shown), suggesting that this gene might be essential for the early specification of the non-neurogenic ectoderm at the anterior and lateral rim of the developing head lobes. Whether this early anterior expression of Pt-pax6.1 is involved in the activation of further eye determination genes remains to be elucidated.
A potential role of peropsins during eye development
We identified a peropsin orthologue in P. tepidariorum that clusters with other chelicerate and vertebrate sequences (Additional file 3: Figure S1). Peropsins are expressed in the retina of several vertebrates [71,72] and amphioxus  where it is proposed to function as a retinal photoisomerase. Clear protostome peropsin orthologues have only been identified in spiders [74,75] and in the American horseshoe crab L. polyphemus . We detect Pt-peropsin expression in the embryonic anlagen of lateral and median eyes, suggesting an early involvement in visual system development or function. Intriguingly, an early function during ocular development has been proposed for peropsins in mice and humans where expression can be detected already during early embryonic stages . Hence, the accessibility of P. tepidariorum development and the availability of functional tools represents an excellent model to further investigate a potential role of peropsins in eye development.
The two eye types in spiders, lateral and median eyes, develop from two different areas in the non-neurogenic ectoderm. Although morphological signs of the eye primordia appear only in the final stages of embryogenesis or later, on the molecular level, the eyes are specified much earlier. Apart from factors that are expressed in all eyes, there are also factors that distinguish the lateral eyes and the median eyes. In addition, among the lateral eyes, the anterior ones are patterned differently from the remaining lateral eyes. The primordia of the median eyes are initially allocated at the anterior rim of the head lobes from where they move to their final location at the anterior rim of the carapace with the non-neural ectoderm that overgrows the underlying brain anlage. All lateral eyes on each side of the head develop from a common eye field, thus providing evidence for the notion that the individual lateral eyes in adult spiders are actually evolutionary remnants of a composite lateral eye. It will be interesting to study the formation and specification of the lateral eyes in spiders in more depth to compare it to the development of the facetted eyes in insects.
anterior lateral eyes
Basic Local Alignment Search Tool
median lateral eyes
posterior lateral eyes
quantitative polymerase chain reaction
retinal determination gene network
We thank Leyli Samadi, Axel Schmid, and Joakim Eriksson for sharing data before publication and for discussions about spider eye development. We also thank Montserrat Torres-Oliva for providing us with the picture of the Drosophila head. We give many thanks to René Illner and Melanie Weber for the help during the initial cloning procedure and in situ hybridizations. This work has been funded by the Deutsche Forschungsgemeinschaft (grants PR1109/4-1 and PR1109/6-1 to NMP), a Junior Group Stipend from the Göttingen Graduate School for Neurosciences, Biophysics and Molecular Biosciences (to NMP) and the Volkswagen Foundation (project number: 85 983; to NP). The open access publication is kindly supported by the German Research Foundation and the Open Access Publication Funds of the Göttingen University.
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