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, 10 (1), 2503

Trilobite Compound Eyes With Crystalline Cones and Rhabdoms Show Mandibulate Affinities

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Trilobite Compound Eyes With Crystalline Cones and Rhabdoms Show Mandibulate Affinities

Gerhard Scholtz et al. Nat Commun.

Abstract

Most knowledge about the structure, function, and evolution of early compound eyes is based on investigations in trilobites. However, these studies dealt mainly with the cuticular lenses and little was known about internal anatomy. Only recently some data on crystalline cones and retinula cells were reported for a Cambrian trilobite species. Here, we describe internal eye structures of two other trilobite genera. The Ordovician Asaphus sp. reveals preserved crystalline cones situated underneath the cuticular lenses. The same is true for the Devonian species Archegonus (Waribole) warsteinensis, which in addition shows the fine structure of the rhabdom in the retinula cells. These results suggest that an apposition eye with a crystalline cone is ancestral for Trilobita. The overall similarity of trilobite eyes to those of myriapods, crustaceans, and hexapods corroborates views of a phylogenetic position of trilobites in the stem lineage of Mandibulata.

Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1
The two major compound eye types of Recent euarthropods. a, b Simplified schemes of the dioptric apparatus of a single unit (ommatidium) of a Recent xiphosuran eye (a) and a Recent mandibulate eye (b). Pigment cells are omitted. Light green: cuticular lens, turquoise: crystalline cone, white: vitreous cells, dark magenta: rhabdom, light magenta: retinula cell bodies gray: cell nuclei. a The cuticular lens forms a cone-like extension. The light is guided via a small transparent vitreous region of about a hundred cells to the rhabdom, i.e. the light-perceiving microvilli of the circularly arranged retinula cells. b A relatively flat cuticular lens is combined with a cellular transparent crystalline cone. The position of the nuclei of the crystalline cones and the retinula cells differ among the mandibulate taxa. c Micrograph of the internal view of a compound eye of the horseshoe crab Limulus polyphemus with numerous cuticular cone-like projections (arrow). d cross-section through the eye of the centipede Scutigera coleoptrata showing biconvex cuticular lenses (le) and the cellular crystalline cones (cc). Scale bars: 200 μm (c), 50 μm (d)
Fig. 2
Fig. 2
The compound eye of Asaphus sp. compared with those of a Recent centipede and xiphosuran. Trilobite images show specimens of the Lindström collection (see Pl. 1, Figs. 28, 30 of Lindström). a, b, c, f, i Synchroton scans of Ar0019635. e, g Semi-thin sections of Ar0059402, j SEM of Ar0019635. a Surface rendering of the Asaphus eye. b Close up of a showing the convex hexagonal facets. c Tangential section of a underneath lenses with putative crystalline cones, indicated by dense filling (arrow), missing cones indicated by dark areas (asterisk). d Cross-section through round crystalline cones surrounded by dark pigment cells of the centipede Scutigera coleoptrata. As in Asaphus these lie underneath hexagonal lenses. e Asaphus tangential section. The white rings correspond to the pointed projections in g. f Transverse section of a. Asterisks mark absent cones, arrows mark ring-like processes. g Cross-section through the eye of Asaphus showing lenses, crystalline cones, displaced crystalline cones (stars), and missing crystalline cones (asterisks). Pointed projections (arrows) form rings surrounding the empty spaces (see e, f). h Transverse section of a S. coleoptrata eye with cuticular lenses and cellular crystalline cones. Arrows point to areas that correspond to the ring-like projections shown in dg. i The fossilized cuticle of Asaphus with pores (arrows). j Section mode (cross-section) of a showing the transition between the thin cuticle of the eye and the thick cuticle of the body. Asterisks mark absent crystalline cones. k Fracture of the exuvia of the xiphosuran Limulus polyphemus. The cone-like projections of the round to hexagonal eye-lenses are part of the endocuticle. The endocuticle of the body is smooth. The exocuticle of the lenses and the body region lie on top. Scale bars 200 μm (a, i), 50 μm (b), 80 μm (c), 30 μm (d), 40 μm (eg), 20 μm (h), 100 μm (j), and 60 μm (k). cc, crystalline cones; cu, cuticle; cub, cuticle of body; cue, cuticle of eyes; enb, endocuticle of body; enle, endocuticle of lenses; exb, exocuticle of body; exle, exocuticle of lenses; le, lenses; m, matrix
Fig. 3
Fig. 3
The compound eye of Archegonus warsteinensis compared with a Recent crustacean eye. Microphotograph (a), μ-CT scan (b, f), SEM (ce, g). a Inner perspective of the eye of A. warsteinensis with the regular arrangement of calcite underneath the cuticular facets. Arrow marks the transition between the eye and body, the cuticle thickens and the calcite shows no regular pattern. Asterisk marks conserved part of the compound eye’s basal membrane. b Surface rendering showing the hexagonal facets. Inset: Section tangential to the eye’s surface revealing the separate putative optical units. c Similar perspective as in (a). The regular pattern of the internal eye parts is visible. Each elongate structure underneath a facet is subdivided into distinct elements, which putatively represent ommatidia. d For comparison, the fracture of an eye of the crustacean Meganyctiphanes norvegica displaying the ommatidial structure: crystalline cones and retinula cells with layered rhabdoms (lenses removed) (after ref. , with permission of the author). Between the crystalline cones and the rhabdom there is a clear zone characteristic of refractive superposition eyes. Asterisk marks the compound eye’s basal membrane (compare with a). e Enlarged part of (c) depicting the details of three putative ommatidia of the fossil trilobite eye. The biconvex lenses (light green) are combined with cone-shaped crystalline cones (turquoise) and adjacent elongate rhabdoms (magenta) resembling those of modern euarthropods (compare with f, g, and Fig. 1b). f Surface rendering of the lens - crystalline cone complex of another part of the eye of A. warsteinensis. The asterisks mark two lenses lacking crystalline cones showing the biconvex form of the lenses and indicating that cones and lenses are separate structures. g The rhabdom of M. norvegica (enlarged from d) revealing a corresponding structure to that of A. warsteinensis (after ref. , with permission of the author). Asterisk marks the basal membrane of the eye. Scale bars 200 μm (a), 150 μm (b), 100 μm (b inset, c), 50 μm (d, f), 20 μm (e), and 10 μm (g). cc, crystalline cones; cz, clear zone; le, lens, rh, rhabdom
Fig. 4
Fig. 4
Simplified cladogram of stem-lineage and crown-group of Euarthropoda (Mandibulata + Chelicerata). The evolutionary key characters of eye evolution are shown (combined from several articles). The ‘other stem-lineage Euarthropoda’ largely comprise the taxa that are sometimes considered as ‘upper-stem Euarthropoda’. Compound eyes with crystalline cones likely evolved in the lineage leading to Trilobita and Mandibulata comprising Myriapoda, Hexapoda, and paraphyletic crustaceans, rendering trilobites part of the mandibulate stem-lineage. Alternative hypotheses about the phylogenetic position of trilobites (stem lineage of Chelicerata or stem-lineage of Euarthropoda) are indicated by dotted lines. If crystalline cones were already present in the compound eyes of Radiodonta, then this character would not be informative with respect to the phylogenetic position of Trilobita. However, this changes to the opposite case if some of the other stem-lineage euarthropods that are more closely related to crown-group euarthropods possessed ommatidia with cuticular cones, as is likely the case for megacheirans

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