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Development Genes and Evolution

, Volume 221, Issue 5–6, pp 329–350 | Cite as

Morphogenesis of Pseudopallene sp. (Pycnogonida, Callipallenidae) II: postembryonic development

  • Georg BrenneisEmail author
  • Claudia P. Arango
  • Gerhard ScholtzEmail author
Original Article

Abstract

Pycnogonida (sea spiders) are bizarre marine arthropods that are nowadays most frequently considered as being the sister group to all other chelicerates. The majority of pycnogonid species develops via a protonymphon larva with only three pairs of limbs affiliated with the future head region. Deviating from this, the hatching stage of some representatives shows already an advanced degree of trunk differentiation. Using scanning electron microscopy, fluorescent nucleic staining, and bright-field stereomicroscopy, postembryonic development of Pseudopallene sp. (Callipallenidae), a pycnogonid with an advanced hatching stage, is described. Based on external morphology, six postembryonic stages plus a sub-adult stage are distinguished. The hatching larva is lecithotrophic and bears the chelifores as only functional appendage pair and unarticulated limb buds of walking leg pairs 1 and 2. Palpal and ovigeral larval limbs are absent. Differentiation of walking leg pairs 3 and 4 is sequential. Apart from the first pair, each walking leg goes through a characteristic sequence of three externally distinct stages with two intermittent molts (limb bud—seven podomeres—nine podomeres). First external signs of oviger development are detectable in postembryonic stage 3 bearing three articulated walking leg pairs. Following three more molts, the oviger has attained adult podomere composition. The advanced hatching stages of different callipallenids are compared and the inclusive term “walking leg-bearing larva” is suggested, as opposed to the behavior-based name “attaching larva”. Data on temporal and structural patterns of walking leg differentiation in other pycnogonids are reviewed and discussed. To facilitate comparisons of walking leg differentiation patterns across many species, we propose a concise notation in matrix fashion. Due to deviating structural patterns of oviger differentiation in another callipallenid species as well as within other pycnogonid taxa, evolutionary conservation of characteristic stages of oviger development is not apparent even in closely related species.

Keywords

Arthropoda Evolution Attaching larva Walking leg Oviger Walking leg-bearing larva 

Notes

Acknowledgments

Karen Gowlett-Holmes and Mick Baron are thanked for sharing their knowledge of Tasmanian dive sites and their invaluable help in collecting Pseudopallene sp. The help of Paul Whitington, Roy Swain, Glenn Johnstone, and Jonny Stark with the logistics of organizing the essential chemicals for processing the developmental stages is greatly appreciated. David Staples kindly provided hatching larvae of Stylopallene cheilorhynchus and S. longicauda. We are grateful to Wilfried Bleiss and Gabriele Drescher for assistance with the scanning electron microscope. Ekaterina Ponomarenko is thanked for the translation of Russian literature.

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).

Supplementary material

427_2011_381_Fig12_ESM.jpg (57 kb)
Supplementary Fig. 1

Walking leg articulation in PS 2 of Pseudopallene sp. Imaris volume, autofluorescent signal. a Walking leg 1, anterior view. The leg possesses the adult number of podomeres, the podomere borders being discernible as regions with higher signal intensity. b Walking leg 2, anterior view. The leg possesses only seven podomeres (including terminal claw), regions of future subdivisions in precursor podomeres are not yet assessable. Note high signal intensity in the cuticular fold relating to the anal opening (arrowhead). cx Coxa, fe femur, pro propodus, ta tarsus, tb tibia, tc terminal claw, wl walking leg (JPEG 57 kb)

427_2011_381_MOESM1_ESM.tif (1.7 mb)
High resolution (TIFF 1,716 kb)
427_2011_381_Fig13_ESM.jpg (124 kb)
Supplementary Fig. 2

Walking leg-bearing larvae of Stylopallene cheilorhynchus and Callipallene sp. SEM micrographs and nucleic stainings. ac S. cheilorhynchus. a Freshly hatched PS 1, anterolateral view. Proboscis and chelifores of the specimen are still inserted in the ripped egg membrane (arrow) and probably an embryonic cuticle. The egg membrane is covered by a hardened sticky matrix via whose stalk-like projection (directed to the left) the egg remains attached to the father’s oviger. The unarticulated limb buds of walking leg 1 and 2 protrude freely from the egg membrane. b PS 1, ventral view. Note the folds of the walking leg tissue beneath the cuticle. c PS 1, posterior view. A tiny interior primordium of walking leg 3 is detectable in the hind body region. The proctodeum/anus is forming beneath the cuticle. The distalmost portion of walking leg 2 will most likely give rise to tarsus and propodus as well as the terminal claw. Proximal to this region, the differentiating tibia 2 may be discernible. df Callipallene sp. d Hatched and still attaching PS1, anterolateral view. Note the elongate anlagen of walking leg pairs 1–3. The arrow indicates a piece of ripped egg membrane (plus part of embryonic cuticle?) that still covers the proboscis and is still attached to the spinning gland of the chelifore. Presumptive podomere regions are labeled along walking leg 1. e PS 1, lateral view, Imaris volume (blend). The spinning gland process is distinctly visible due to its autofluorescent signal. A shallow elevation of the developing ocular tubercle lies slightly anterior to walking leg 1. Note the primordium of walking leg 4 as well as the interior tissue folds of walking legs 1–3 that may partially directly relate to the borders of future leg podomeres. f PS 1, ventral view. Walking leg pair 3 is bent in an anterior direction, being wedged between walking leg pairs 1 and 2. The primordium of walking leg pair 4 is already externally detectable, flanking the hind body region that still lacks an anus. ch chelifore, cx coxa, fe femur, ot ocular tubercle, pr proboscis, pro propodus, sgp spinning gland process, ta tarsus, tb tibia, tc terminal claw, wl walking leg (JPEG 124 kb)

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Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Humboldt-Universität zu BerlinInstitut für Biologie/Vergleichende ZoologieBerlinGermany
  2. 2.Biodiversity ProgramQueensland MuseumSouth BrisbaneAustralia

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