Letter

Nature 437, 1144-1148 (20 October 2005) | doi:10.1038/nature03984; Received 10 February 2005; Accepted 30 June 2005

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

Amy Maxmen1, William E. Browne3, Mark Q. Martindale3 & Gonzalo Giribet2

  1. Department of Organismic & Evolutionary Biology and Museum of Comparative Zoology, Harvard University, 26 Oxford Street,
  2. Department of Organismic & Evolutionary Biology and Museum of Comparative Zoology, Harvard University, 16 Divinity Avenue, Cambridge, Massachusetts 02138, USA
  3. Kewalo Marine Lab, Pacific Biosciences Research Center, University of Hawaii, 41 Ahui Street, Honolulu, Hawaii 96813, USA

Correspondence to: Amy Maxmen1 Correspondence and requests for materials should be addressed to A.M. (Email: amaxmen@oeb.harvard.edu).

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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