The development of the nervous system in Laevicaudata (Crustacea, Branchiopoda): insights into the evolution and homologies of branchiopod limbs and ‘frontal organs’

Abstract

We investigated the development of the external morphology and of the nervous system in Lynceus biformis and Lynceus brachyurus (Laevicaudata, Branchiopoda), by using immunohistochemical methods in combination with a confocal laser scanning analysis. In both Lynceus species, a free-swimming nauplius larva, equipped with three appendages, hatches from resting eggs. Despite their close phylogenetic relationship to each other, considerable differences are present in their external morphology. Hatching L. brachyurus larvae are equipped with a large and flattened labrum, where in contrast, the L. biformis larvae possess a smaller labrum with four conspicuous posteriorly directed spines at its margin. Despite these differences, the development of the nervous system is quite similar in both species. The hatching larvae are equipped with a naupliar nervous system, and only in the more advanced stages, the development of the ventral nerve cord starts. Furthermore, our investigation into the nervous system provided insights into architecture and evolution of protocerebral sensory organs, the dorsal setae field and the dorsal frontal organ, only present in Laevicaudata. The identification of frontal filaments with an associated frontal filament organ in Lynceus revealed—after a comprehensive comparison with other branchiopods—that these organs exist throughout Branchiopoda and are comparable to those in other crustaceans. Additionally, our results of the peripheral nervous system analysis showed that the innervation pattern of the naupliar appendages (antenna and mandible) and the trunk appendages could be serially homologized, despite much difference in gross morphology of these. Based on the innervation pattern of limbs, we suggest that the larval uniramous mandibular palp, found in the larvae of all ‘large’ branchiopods, is largely exopodal of nature (contrary to most earlier statements) and that the endopodite of the trunk limbs consists of only one distal endite-like segment (confirming some earlier statements) and not of three as proposed by others.

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Note added in proof

Weiss et al. (2012) describe the nervous system in certain Daphnia species. They show the presence of frontal filaments and of a dorsal frontal organ. The latter, however, does not correspond to the dorsal frontal organ described herein in Laevicaudata. Morphology of the Daphnia Nervous System: A Comparative Study on Daphnia pulex, Daphnia lumholtzi, and Daphnia longicephala L. C. Weiss, R. Tollrian, Z. Herbert, C. Laforsch. J Morphol. DOI: 10.1002/jmor.20068.

Acknowledgments

The authors would like to thank Mark J. Grygier, guiding Tomonari Kaji to the Lynceus biformis locality. The ‘Deutsche Forschungsgemeinschaft’ is acknowledged for financial support to Stefan Richter (RI 837/9-1, 2). Two anonymous reviewers provided helpful comments and Lucy Cathrow improved the English.

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Correspondence to Martin Fritsch.

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Communicated by A. Schmidt-Rhaesa.

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Fritsch, M., Kaji, T., Olesen, J. et al. The development of the nervous system in Laevicaudata (Crustacea, Branchiopoda): insights into the evolution and homologies of branchiopod limbs and ‘frontal organs’. Zoomorphology 132, 163–181 (2013). https://doi.org/10.1007/s00435-012-0173-0

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Keywords

  • Dorsal setae field
  • Fluorescence microscopy
  • Frontal filament organ
  • Lynceus nervous system
  • Serial limb homology