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Remnants of ancestral larval eyes in an eyeless mollusk? Molecular characterization of photoreceptors in the scaphopod Antalis entalis.

ABSTRACT: Background:Eyes have evolved and been lost multiple times during animal evolution, however, the process of eye loss has only been reconstructed in a few cases. Mollusks exhibit eyes as varied as the octopod camera eye or the gastropod cup eye and are ideal systems for studying the evolution of eyes, photoreceptors, and opsins. Results:Here, we identify genes related to photoreceptor formation and function in an eyeless conchiferan mollusk, the scaphopod Antalis entalis, and investigate their spatial and temporal expression patterns during development. Our study reveals that the scaphopod early mid-stage trochophore larva has putative photoreceptors in a similar location and with a similar gene expression profile as the trochophore of polyplacophoran mollusks. The apical and post-trochal putative photoreceptors appear to co-express go-opsin, six1/2, myoV, and eya, while expression domains in the posterior foot and pavilion (posterior mantle opening) show co-expression of several other candidate genes but not go-opsin. Sequence analysis reveals that the scaphopod Go-opsin amino acid sequence lacks the functionally important lysine (K296; Schiff base) in the retinal-binding domain, but has not accumulated nonsense mutations and still exhibits the canonical G-protein activation domain. Conclusions:The scaphopod Go-opsin sequence reported here is the only known example of a bilaterian opsin that lacks lysine K296 in the retinal-binding domain. Although this may render the Go-opsin unable to detect light, the protein may still perform sensory functions. The location, innervation, development, and gene expression profiles of the scaphopod and polyplacophoran apical and post-trochal photoreceptors suggest that they are homologous, even though the scaphopod post-trochal photoreceptors have degenerated. This indicates that post-trochal eyes are not a polyplacophoran apomorphy but likely a molluscan synapomorphy lost in other mollusks. Scaphopod eye degeneration is probably a result of the transition to an infaunal life history and is reflected in the likely functional degeneration of Go-opsin, the loss of photoreceptor shielding pigments, and the scarce expression of genes involved in phototransduction and eye development. Our results emphasize the importance of studying a phylogenetically broad range of taxa to infer the mechanisms and direction of body plan evolution.

SUBMITTER: Wollesen T

PROVIDER: S-EPMC6800502 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Remnants of ancestral larval eyes in an eyeless mollusk? Molecular characterization of photoreceptors in the scaphopod <i>Antalis entalis</i>.

Wollesen Tim T McDougall Carmel C Arendt Detlev D

EvoDevo 20191019

<h4>Background</h4>Eyes have evolved and been lost multiple times during animal evolution, however, the process of eye loss has only been reconstructed in a few cases. Mollusks exhibit eyes as varied as the octopod camera eye or the gastropod cup eye and are ideal systems for studying the evolution of eyes, photoreceptors, and opsins.<h4>Results</h4>Here, we identify genes related to photoreceptor formation and function in an eyeless conchiferan mollusk, the scaphopod <i>Antalis entalis</i>, and ...[more]

PMID: 31641428

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Project description:BackgroundEyes in bilaterian metazoans have been described as being composed of either ciliary or rhabdomeric photoreceptors. Phylogenetic distribution, as well as distinct morphologies and characteristic deployment of different photopigments (ciliary vs. rhabdomeric opsins) and transduction pathways argue for the co-existence of both of these two photoreceptor types in the last common bilaterian ancestor. Both receptor types exist throughout the Bilateria, but only vertebrates are thought to use ciliary photoreceptors for directional light detection in cerebral eyes, while all other invertebrate bilaterians studied utilize rhabdomeric photoreceptors for this purpose. In protostomes, ciliary photoreceptors that express c-opsin have been described only from a non-visual deep-brain photoreceptor. Their homology with vertebrate rods and cones of the human eye has been hypothesized to represent a unique functional transition from non-visual to visual roles in the vertebrate lineage.ResultsTo test the hypothesis that protostome cerebral eyes employ exclusively rhabdomeric photoreceptors, we investigated the ultrastructure of the larval eyes in the brachiopod Terebratalia transversa. We show that these pigment-cup eyes consist of a lens cell and a shading pigment cell, both of which are putative photoreceptors, deploying a modified, enlarged cilium for light perception, and have axonal connections to the larval brain. Our investigation of the gene expression patterns of c-opsin, Pax6 and otx in these eyes confirms that the larval eye spots of brachiopods are cerebral eyes that deploy ciliary type photoreceptors for directional light detection. Interestingly, c-opsin is also expressed during early embryogenesis in all potential apical neural cells, becoming restricted to the anterior neuroectoderm, before expression is initiated in the photoreceptor cells of the eyes. Coincident with the expression of c-opsin in the presumptive neuroectoderm, we found that middle gastrula stage embryos display a positive photoresponse behavior, in the absence of a discrete shading pigment or axonal connections between cells.ConclusionsOur results indicate that the dichotomy in the deployment of ciliary and rhabdomeric photoreceptors for directional light detection is not as clear-cut as previously thought. Analyses of brachiopod larval eyes demonstrate that the utilization of c-opsin expressing ciliary photoreceptors in cerebral eyes is not limited to vertebrates. The presence of ciliary photoreceptor-based eyes in protostomes suggests that the transition between non-visual and visual functions of photoreceptors has been more evolutionarily labile than previously recognized, and that co-option of ciliary and rhabdomeric photoreceptor cell types for directional light detection has occurred multiple times during animal evolution. In addition, positive photoresponse behavior in gastrula stage embryos suggests that a discrete shading pigment is not requisite for directional photoreception in metazoans. Scanning photoreception of light intensities mediating cell-autonomous changes of ciliary movement may represent an ancient mechanism for regulating locomotory behavior, and is likely to have existed prior to the evolution of eye-mediated directional light detection employing axonal connections to effector cells and a discreet shading pigment.

Project description:BACKGROUND:Development of cerebral eyes is generally based on fine-tuned networks and closely intertwined with the formation of brain and head. Consistently and best studied in insects and vertebrates, many signaling pathways relaying the activity of eye developmental factors to positional information in the head region are characterized. Though known from several organisms, photoreceptors developing outside the head region are much less studied and the course of their development, relation to cerebral eyes and evolutionary origin is in most cases unknown. To explore how position influences development of otherwise similar photoreceptors, we analyzed the molecular characteristics of photoreceptors we discovered at the very anterior, the posttrochal mid-body and posterior body region of larval Leptochiton asellus, a representative of the chiton subgroup of mollusks. RESULTS:Irrespective of their position, all found photoreceptors exhibit a molecular signature highly similar to cerebral eye photoreceptors of related animals. All photoreceptors employ the same subtype of visual pigments (r-opsin), and the same key elements for phototransduction such as GNAq, trpC and arrestin and intracellular r-opsin transport such as rip11 and myosinV as described from other protostome cerebral eyes. Several transcription factors commonly involved in cerebral eye and brain development such as six1/2, eya, dachshund, lhx2/9 and prox are also expressed by all found photoreceptor cells, only pax6 being restricted to the anterior most cells. Coexpression of pax6 and MITF in photoreceptor-associated shielding pigment cells present at the mid-body position matches the common situation in cerebral eye retinal pigment epithelium specification and differentiation. Notably, all photoreceptors, even the posterior ones, further express clear anterior markers such as foxq2, irx, otx, and six3/6 (only the latter absent in the most posterior photoreceptors), which play important roles in the early patterning of the anterior neurogenic area throughout the animal kingdom. CONCLUSIONS:Our data suggest that anterior eyes with brain-associated development can indeed be subject to heterotopic replication to developmentally distinct and even posterior body regions. Retention of the transcriptional activity of a broad set of eye developmental factors and common anterior markers suggests a mode of eye development induction, which is largely independent of body regionalization.

Dataset Information

Remnants of ancestral larval eyes in an eyeless mollusk? Molecular characterization of photoreceptors in the scaphopod Antalis entalis.

Publications

Remnants of ancestral larval eyes in an eyeless mollusk? Molecular characterization of photoreceptors in the scaphopod <i>Antalis entalis</i>.

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