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Neuroanatomy of sea spiders implies an appendicular origin of the protocerebral segment

Nature volume 437, pages 1144–1148 (2005)Cite this article

Abstract

Independent specialization of arthropod body segments has led to more than a century of debate on the homology of morphologically diverse segments1,2, each defined by a lateral appendage and a ganglion of the central nervous system. The plesiomorphic composition of the arthropod head remains enigmatic because variation in segments and corresponding appendages is extreme. Within extant arthropod classes (Chelicerata, Myriapoda, Crustacea and Hexapoda—including the insects), correspondences between the appendage-bearing second (deutocerebral) and third (tritocerebral) cephalic neuromeres have been recently resolved on the basis of immunohistochemistry1 and Hox gene expression patterns3,4. However, no appendage targets the first ganglion, the protocerebrum, and the corresponding segmental identity of this anterior region remains unclear5. Reconstructions of stem-group arthropods indicate that the anteriormost region originally might have borne an ocular apparatus and a frontal appendage innervated by the protocerebrum6. However, no study of the central nervous system in extant arthropods has been able to corroborate this idea directly, although recent analyses of cephalic gene expression patterns in insects suggest a segmental status for the protocerebral region7,8,9,10. Here we investigate the developmental neuroanatomy of a putative basal arthropod11, the pycnogonid sea spider, with immunohistochemical techniques. We show that the first pair of appendages, the chelifores, are innervated at an anterior position on the protocerebrum. This is the first true appendage shown to be innervated by the protocerebrum, and thus pycnogonid chelifores are not positionally homologous to appendages of extant arthropods but might, in fact, be homologous to the ‘great appendages’ of certain Cambrian stem-group arthropods.

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Figure 1: Proposed relationships of pycnogonids among other ecdysozoans.
Figure 2: The unique adult and larval morphology of pycnogonids.
Figure 3: CNS of the Anoplodactylus sp. larva (protonymphon).

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Acknowledgements

We thank W. Morrisey for diagram preparation; E. C. Seaver for assistance with immunohistochemistry; and J. Hanken, G. Das, G. Edgecombe and A. Hejnol for advice and discussion. We thank the Developmental Studies Hybridoma Bank for the anti-tubulin and Elav antibodies. This material is based on work supported by the National Science Foundation AToL program to G.G. and M.Q.M.

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Authors and Affiliations

  1. Department of Organismic & Evolutionary Biology and Museum of Comparative Zoology, Harvard University, 26 Oxford Street,

    Amy Maxmen

  2. Department of Organismic & Evolutionary Biology and Museum of Comparative Zoology, Harvard University, 16 Divinity Avenue, Massachusetts, 02138, Cambridge, USA

    Gonzalo Giribet

  3. Kewalo Marine Lab, Pacific Biosciences Research Center, University of Hawaii, 41 Ahui Street, Hawaii, 96813, Honolulu, USA

    William E. Browne & Mark Q. Martindale

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Correspondence to Amy Maxmen.

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Supplementary information

Supplementary Video 1

The nervous system of an Anoplodactylus protonymphon larva (anti-tubulin (red) and anti-serotonin 5HT (green)), corresponding to text Figure 3b. Anterior chelifores are directed towards the upper right corner. The pair of bifurcating ocular nerves exit the protocerebral commissure dorsally. The rotating projection has been obtained by converting a z-stack of cLSM images into a projection using Zeiss LSM 510 software. (MOV 1652 kb)

Supplementary Figure 2

These images show an Anoplodactylus larva labelled with the neuronal marker, Elav (red). Anterior chelifores are directed up. The ocular nerves exiting the dorsal surface of the protocerebrum have been converted from red to yellow. A. Scale bar: 25 µm. In the upper row, ocular nerves are artificially coloured, the bottom row is raw data. (PDF 950 kb)

Supplementary Video 2b

The innervated esophagus has been converted to greyscale. The spatial relationships of neuropil ring components are visible by scrolling through a z-stack of cLSM images captured incrementally between the ventral to dorsal surface of the protonymphon (MOV 1461 kb)

Supplementary Video 2c

The spatial relationships of neuropil ring components are visible via rotating projection of the z-stack created using Zeiss LSM software. (MOV 2238 kb)

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Maxmen, A., Browne, W., Martindale, M. et al. Neuroanatomy of sea spiders implies an appendicular origin of the protocerebral segment. Nature 437, 1144–1148 (2005). https://doi.org/10.1038/nature03984

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