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Expression of Distal-less, dachshund, and optomotor blind in Neanthes arenaceodentata (Annelida, Nereididae) does not support homology of appendage-forming mechanisms across the Bilateria

Winchell, Christopher J. and Valencia, Jonathan E. and Jacobs, David K. (2010) Expression of Distal-less, dachshund, and optomotor blind in Neanthes arenaceodentata (Annelida, Nereididae) does not support homology of appendage-forming mechanisms across the Bilateria. Development genes and evolution, 220 (9-10). pp. 275-295. ISSN 0949-944X . http://resolver.caltech.edu/CaltechAUTHORS:20110208-085943578

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Abstract

The similarity in the genetic regulation of arthropod and vertebrate appendage formation has been interpreted as the product of a plesiomorphic gene network that was primitively involved in bilaterian appendage development and co-opted to build appendages (in modern phyla) that are not historically related as structures. Data from lophotrochozoans are needed to clarify the pervasiveness of plesiomorphic appendage forming mechanisms. We assayed the expression of three arthropod and vertebrate limb gene orthologs, Distal-less (Dll), dachshund (dac), and optomotor blind (omb), in direct-developing juveniles of the polychaete Neanthes arenaceodentata. Parapodial Dll expression marks premorphogenetic notopodia and neuropodia, becoming restricted to the bases of notopodial cirri and to ventral portions of neuropodia. In outgrowing cephalic appendages, Dll activity is primarily restricted to proximal domains. Dll expression is also prominent in the brain. dac expression occurs in the brain, nerve cord ganglia, a pair of pharyngeal ganglia, presumed interneurons linking a pair of segmental nerves, and in newly differentiating mesoderm. Domains of omb expression include the brain, nerve cord ganglia, one pair of anterior cirri, presumed precursors of dorsal musculature, and the same pharyngeal ganglia and presumed interneurons that express dac. Contrary to their roles in outgrowing arthropod and vertebrate appendages, Dll, dac, and omb lack comparable expression in Neanthes appendages, implying independent evolution of annelid appendage development. We infer that parapodia and arthropodia are not structurally or mechanistically homologous (but their primordia might be), that Dll’s ancestral bilaterian function was in sensory and central nervous system differentiation, and that locomotory appendages possibly evolved from sensory outgrowths.


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http://dx.doi.org/10.1007/s00427-010-0346-0DOIUNSPECIFIED
http://www.springerlink.com/content/k68182x432n67403/PublisherUNSPECIFIED
Additional Information:© 2010 The Authors. This article is published with open access at Springerlink.com. This article is distributed under the terms of the Creative Commons Attribution Noncommercial License which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited. Received: 26 July 2010, Accepted: 9 November 2010, Published online: 30 November 2010. Communicated by D.A. Weisblat. We thank Elaine Seaver for technical advice, Volker Hartenstein for discussion and use of sectioning equipment, and two anonymous reviewers for their valuable suggestions. This work was supported by a GAANN fellowship to CJW and NASA Astrobiology funding to DKJ.
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Funding AgencyGrant Number
Graduate Assistance in Areas of National Need (GAANN)UNSPECIFIED
NASAUNSPECIFIED
Subject Keywords:Polychaete, Appendages, Nervous system, Distal-less, dachshund, optomotor blind
Record Number:CaltechAUTHORS:20110208-085943578
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20110208-085943578
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:22066
Collection:CaltechAUTHORS
Deposited By: Benjamin Perez
Deposited On:08 Feb 2011 18:35
Last Modified:26 Dec 2012 12:54

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