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Morphogenesis of Pseudopallene sp. (Pycnogonida, Callipallenidae) I: embryonic development

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Abstract

Embryonic development of Pycnogonida (sea spiders) is poorly understood in comparison to other euarthropod lineages with well-established model organisms. However, given that pycnogonids potentially represent the sister group to chelicerates or even to all other euarthropods, their development might yield important data for the reconstruction of arthropod evolution. Using scanning electron microscopy, fluorescent nucleic staining and immunohistochemistry, the general course of embryonic morphogenesis in Pseudopallene sp. (Callipallenidae), a pycnogonid with prolonged embryonic development, is described. A staging system comprising ten stages is presented, which can be used in future studies addressing specific developmental processes. The initially slit-like stomodeum anlage forms at the anterior end of an eight-shaped germ band and predates proboscis outgrowth. The latter process is characterized by the protrusion of three cell populations that are subsequently involved in pharynx formation. In later stages, the proboscis assumes distally a horseshoe-like shape. At no time, a structure corresponding to the euarthropod labrum is detectable. Based on the complete lack of palpal and ovigeral embryonic limbs and the early differentiation of walking leg segments 1 and 2, the existence of an embryonized protonymphon stage during callipallenid development is rejected. The evolution of pycnogonid hatching stages, especially within Callipallenidae and Nymphonidae, is re-evaluated in the light of recent phylogenetic analyses. Specifically, the re-emergence of the ancestral protonymphon larva (including re-development of palpal and ovigeral larval limbs) and a possible re-appearance of adult palps in the nymphonid lineage are discussed. This challenges the perception of pycnogonid head appendage evolution as being driven by reduction events alone.

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Acknowledgments

Karen Gowlett-Holmes and Mick Baron are thanked for sharing their knowledge of Tasmanian dive sites and their invaluable help in specimen collection. The help of Paul Whitington, Roy Swain, Glenn Johnstone and Jonny Stark with the logistics of organizing the essential chemicals for processing embryos and larval stages is greatly appreciated. We are grateful to Wilfried Bleiss and Gabriele Drescher for the assistance with the scanning electron microscope. Petra Ungerer is thanked for critically reading parts of an earlier version of the manuscript. Collection of animals and their offspring was made possible by permits of the Tasmanian Department of Primary Industries, Parks, Water and Environment (permit nos. 6039 and 9255). Export of collected material was permitted by the Australian Department of the Environment, Water, Heritage and the Arts (permit nos. WT2008-4394 and WT2009-4260). GB was in part supported by the Studienstiftung des deutschen Volkes, and CPA was supported by Australian Biological Resources Study (ABRS, grant 204–61). The project was funded by the Deutsche Forschungsgemeinschaft (Scho 442/13-1)

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  1. Humboldt-Universität zu Berlin, Institut für Biologie/Vergleichende Zoologie, Philippstraße 13, 10115, Berlin, Germany

    Georg Brenneis & Gerhard Scholtz

  2. Biodiversity Program, Queensland Museum, P.O. Box 3300, South Brisbane, Queensland, 4101, Australia

    Claudia P. Arango

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  1. Georg Brenneis
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Stomodeal cell immigration in ES 2 of Pseudopallene sp. Tubulin labeling (orange) with nucleic counterstain (green), Imaris volume (blend), same embryo as shown in Fig. 2c. The movie starts from anteroventral view, the embryo turns first in ventral then in lateral direction. Anteriorly in the germ band, a median tubulin-positive region is found where cells of the future stomodeum immigrate. The semicircular furrows of the chelifore anlagen are only indistinctly recognizable. An optical clipping plane along the sagittal axis of the embryo reveals the interiorly displaced nuclei of the immigrating stomodeal cells. (MPG 5076 kb)

Detail of the outgrowing proboscis in ES 4 of Pseudopallene sp. Tubulin labeling (orange) with nucleic counterstain (green), Imaris volume (blend). The movie starts from ventral view, the embryo rotates first laterally then dips backwards. The arrangement of the three cell populations creates the characteristic Y-shaped pharynx lumen. A distinct ring-like ridge of surrounding ectodermal cells starts to cover these cell populations (compare to Fig. 3g). At this stage, the medially touching chelifore anlagen are still positioned fully posterior to the proboscis. (MPG 7196 kb)

Detail of proboscis in ES 7 of Pseudopallene sp. Tubulin labeling (orange) with nucleic counterstain (green), Imaris volume (blend). The movie starts from ventral view, the embryo rotates first laterally then dips backwards. The developing mouth opening has a triangular shape. A distinct notch is found at the posterior margin of the proboscis, giving its distalmost portion a horseshoe-like appearance. The chelifore scapes that flank the proboscis laterally are damaged in this particular embryo. (MPG 6646 kb)

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Brenneis, G., Arango, C.P. & Scholtz, G. Morphogenesis of Pseudopallene sp. (Pycnogonida, Callipallenidae) I: embryonic development. Dev Genes Evol 221, 309–328 (2011). https://doi.org/10.1007/s00427-011-0382-4

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