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Abstract Complex biological traits often originate by integrating previously separate parts, but the organismal functions of these precursors are challenging to infer. If we can understand the ancestral functions of these precursors, it could help explain how they persisted and how they facilitated the origins of complex traits. Animal eyes are some of the best studied complex traits, and they include many parts, such as opsin‐based photoreceptor cells, pigment cells, and lens cells. Eye evolution is understood through conceptual models that argue these parts gradually came together to support increasingly sophisticated visual functions. Despite the well‐accepted logic of these conceptual models, explicit comparative studies to identify organismal functions of eye precursors are lacking. Here, we investigate how precursors functioned before they became part of eyes in Cnidaria, a group formed by sea anemones, corals, and jellyfish. Specifically, we test whether ancestral photoreceptor cells regulated the discharge of cnidocytes, the expensive single‐use cells with various functions including prey capture, locomotion, and protection. Similar to a previous study ofHydra, we show an additional four distantly related cnidarian groups discharge significantly more cnidocytes when exposed to dim blue light compared with bright blue light. Our comparative analyses support the hypothesis that the cnidarian ancestor was capable of modulating cnidocyte discharge with light, which we speculate uses an opsin‐based phototransduction pathway homologous to that previously described inHydra. Although eye precursors might have had other functions like regulating timing of spawning, our findings are consistent with the hypothesis that photoreceptor cells which mediate cnidocyte discharge predated eyes, perhaps facilitating the prolific origination of eyes in Cnidaria.
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Expression of Opsins of the Box Jellyfish Tripedalia cystophora Reveals the First Photopigment in Cnidarian Ocelli and Supports the Presence of Photoisomerases
Cubomedusae, or box jellyfish, have a complex visual system comprising 24 eyes of four types. Like other cnidarians, their photoreceptor cells are ciliary in morphology, and a range of different techniques together show that at least two of the eye types—the image-forming upper and lower lens eyes—express opsin as the photopigment. The photoreceptors of these two eye types express the same opsin ( Tc LEO ), which belongs to the cnidarian-specific clade cnidops. Interestingly, molecular work has found a high number of opsin genes in box jellyfish, especially in the Caribbean species Tripedalia cystophora , most of which are of unknown function. In the current study, we raised antibodies against three out of five opsins identified from transcriptomic data from T. cystophora and used them to map the expression patterns. These expression patterns suggest one opsin as the photopigment in the slit eyes and another as a putative photoisomerase found in photoreceptors of all four eyes types. The last antibody stained nerve-like cells in the tentacles, in connection with nematocytes, and the radial nerve, in connection with the gonads. This is the first time photopigment expression has been localized to the outer segments of the photoreceptors in a cnidarian ocellus (simple eye). The potential presence of a photoisomerase could be another interesting convergence between box jellyfish and vertebrate photoreceptors, but it awaits final experimental proof.
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- Award ID(s):
- 2153773
- PAR ID:
- 10414432
- Date Published:
- Journal Name:
- Frontiers in Neuroanatomy
- Volume:
- 16
- ISSN:
- 1662-5129
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/fnana.2022.916510
