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, 107 (52), 22576-81

Expression Patterns of Neural Genes in Euperipatoides Kanangrensis Suggest Divergent Evolution of Onychophoran and Euarthropod Neurogenesis

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Expression Patterns of Neural Genes in Euperipatoides Kanangrensis Suggest Divergent Evolution of Onychophoran and Euarthropod Neurogenesis

Bo Joakim Eriksson et al. Proc Natl Acad Sci U S A.

Abstract

One of the controversial debates on euarthropod relationships centers on the question as to whether insects, crustaceans, and myriapods (Mandibulata) share a common ancestor or whether myriapods group with the chelicerates (Myriochelata). The debate was stimulated recently by studies in chelicerates and myriapods that show that neural precursor groups (NPGs) segregate from the neuroectoderm generating the nervous system, whereas in insects and crustaceans the nervous tissue is produced by stem cells. Do the shared neural characters of myriapods and chelicerates represent derived characters that support the Myriochelata grouping? Or do they rather reflect the ancestral pattern? Analyses of neurogenesis in a group closely related to euarthropods, the onychophorans, show that, similar to insects and crustaceans, single neural precursors are formed in the neuroectoderm, potentially supporting the Myriochelata hypothesis. Here we show that the nature and the selection of onychophoran neural precursors are distinct from euarthropods. The onychophoran nervous system is generated by the massive irregular segregation of single neural precursors, contrasting with the limited number and stereotyped arrangement of NPGs/stem cells in euarthropods. Furthermore, neural genes do not show the spatiotemporal pattern that sets up the precise position of neural precursors as in euarthropods. We conclude that neurogenesis in onychophorans largely does not reflect the ancestral pattern of euarthropod neurogenesis, but shows a mixture of derived characters and ancestral characters that have been modified in the euarthropod lineage. Based on these data and additional evidence, we suggest an evolutionary sequence of arthropod neurogenesis that is in line with the Mandibulata hypothesis.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
(A–E) Formation of neuromeres in the E. kanangrensis embryo. Light micrographs of transverse sections through the ventral neuroectoderm; dorsal is toward the top. Asterisks (*) label neuroecodermal cells. Some of the segregating neural precursors are outlined in black. (A) Stage II, single neural precursors (arrows) delaminate from the neuroectoderm (*) and form a loose basal layer between the outer ectoderm and the inner mesoderm. Before delamination, the neural precursors assume a bottle-like shape (arrowheads). (B) Neural precursors divide to generate smaller intermediate neural precursors (arrows). (C) Due to the segregation of additional neural precursors, the basal layer increases (arrows). (D) At stage III, the neuropile is visible surrounded by differentiated neurons (large arrowheads). Small arrowheads point to intermediate neural precursors; arrow indicates a segregated precursor. (E) At stage IV, the basal area of differentiating neurons has expanded, whereas the size of the neural precursor and intermediate neural precursor layers remains the same. Large arrowhead indicates a differentiated neuron; small arrowheads point to intermediate neural precursors; arrowhead points to a segregated precursor. ms, mesoderm; np, neuropile. (Scale bars: 25 μm in A–C; 50 μm in D and E.)
Fig. 2.
Fig. 2.
(A–K) Proliferation and segregation pattern of neural precursors. Confocal micrographs of flat preparations of embryos at stage IV stained with phalloidin (red) and anti–phospho-histone 3 (blue) (A–G) and schematic drawings of neural precursors (H–K); anterior is toward the left in A–C and toward the top in D–K. (A) Mitotic cells (arrow) in the ventral neuroectoderm. (B and C) Formation of the ganglion anlage; the arrowheads indicate the segmental borders. Arrow in B points to proliferating intermediate neural precursors; arrow in C points to a dividing neuroectodermal cell. (D–G) Optical horizontal sections through the developing neuromere of the 2. walking leg segment of a stage IV embryo at different apico-basal levels (1–13 μm). Arrow in D indicates a dividing neuroectodermal cell; arrows in E–G point to segregated neural precursors; arrowhead in G indicates a dividing neural precursor. Inset in G shows a higher magnification of dividing neural precursors (arrowheads). (H–K) Pattern of segregated neural precursors in three consecutive hemisegments of the same embryo, representing consecutive developmental stages (stage IV/1–3) and the segregation pattern in an older embryo (stage IV/late). Each schematic drawing represents the distribution of segregated neural precursors in a single hemineuromere and is based on the analysis of stacks of 34–70 horizontal sections depending on the thickness of the neuromeres, which increases over time (Fig. S1). A, anterior; l1 to l4, developing neuromeres of walking leg segments 1–4; P, posterior. (Scale bars: 50 μm in A and D–G; 25 μm in B and C.)
Fig. 3.
Fig. 3.
(A–F) Expression pattern of EkASH. Light micrographs of flat preparations (A–D) and transverse sections (E and F) of embryos stained with a DIG-labeled EkASH probe; anterior is toward the left in A–D, dorsal is toward the top in E and F. (A and B) Ventral views show that EkASH expression is homogeneous in the neuroectoderm. Transcripts are up-regulated in segregated neural precursors (arrows). Circles indicate the position of the limb buds. Arrowheads in B indicate the area between the neuromeres which shows low/absent levels of EkASH. (C and D) Sagittal views show that EkASH is expressed at low, homogenous levels in the neuroectoderm but is strongly expressed in the segregated neural precursors (arrows). Arrowhead indicates the area between the developing neuromeres. (E and F) EkASH is strongly expressed in the segregated neural precursors (arrow in E) and the intermediate precursors (arrowhead in F). l1 to l4, developing neuromeres of walking leg segments 1–4; ml, ventral midline; ms, mesoderm; vne, ventral neuroectoderm. (Scale bars: 100 μm in A, 100 μm in B, 50 μm in C, and 50 μm in E and F.)
Fig. 4.
Fig. 4.
(A–E) Expression pattern of EkDelta. Light micrographs of flat preparations (A–E) and transverse sections (E) of embryos stained with a DIG-labeled EkDelta probe; anterior is toward the left in A–D, dorsal is toward the top in E. (A–C) EkDelta is strongly expressed in the ventral neuroectoderm (arrows). Expression is lower between the developing neuromeres (arrowheads). EkDelta is expressed in the sensory organ precursors. (D) Sagittal view of a stage II embryo shows that EkDelta is expressed in the ventral neuroectoderm, segregated neural precursors, and mesoderm. Arrowheads indicate area between segments. (E) At stage IV, EkDelta is expressed in the ventral neuroectoderm and segregated (arrows) and intermediate neural precursors (arrowheads) l1 to l6, developing neuromeres of walking leg segments 1–6; ml, ventral midline; ms, mesoderm; sop, sensory organ precursors; vne, ventral neuroectoderm. (Scale bars: A. 100 μm; B, 50 μm; C, 100 μm; D, 50 μm; and E, 50 μm.)
Fig. 5.
Fig. 5.
(A–C) Expression pattern of EkNotch. Light micrographs of flat preparations (A and B) and transverse section (C) of embryos stained with DIG-labeled EkNotch probe; anterior is toward the left in A and C; dorsal is toward the top in B. (A and C) EkNotch is expressed homogenously in the ventral neuroectoderm (arrows). (B) In addition, EkNotch is expressed in the segregated (arrow) and intermediate neural precursors (arrowhead), the neuropile and the most basal differentiating neurons (small arrowheads), and the mesoderm (small arrows). l1, l9 to l11, developing neuromeres of walking leg segments 9–11; ml, ventral midline; ms, mesoderm; vne, ventral neuroectoderm. (Scale bars: A and C, 100 μm; B, 50 μm.)

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