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

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 pre-morphogenetic 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.

Stable transgenesis in the marine annelid Platynereis dumerilii sheds new light on photoreceptor evolution

“…Next, we assessed if there are other transcription factors correlating with the development of noncephalic r-opsin cells in the regenerates. Dach was previously only reported for its expression in Platynereis mushroom bodies (32), but in a related polychaete, Neanthes arenaceodentata, it also prominently labels cells in the VNC and at the base of each parapodium (33). In adult Platynereis specimens, dach is weakly detectable in dispersed cells of the ventral trunk.…”

Echinodermata

“…Insights into the affi nity of the echinoderm ambulacrum are provided by data on expression of some regulatory genes during development, in particular the homologs of distal-less , which is normally expressed in the growing tips of several bilaterian appendages (e.g., annelid parapodia, tunicate ampullae, vertebrate limb buds) and in the podia of larval and juvenile echinoderms Panganiban et al 1997 ), although these expression data alone do not suffi ciently argue for homology of echinoderm podia to other bilaterian appendages (e.g., (Winchell et al 2010 ).…”

Evolutionary crossroads in developmental biology: annelids

“…Development 139 (15) PRIMER Development 139 (15) et al, 2004), gut (Arendt et al, 2001;Boyle and Seaver, 2008;Saudemont et al, 2008;Hui et al, 2009;Boyle and Seaver, 2010), appendages (Panganiban et al, 1997;Winchell et al, 2010;McDougall et al, 2011), mesoderm (Kerner et al, 2006;Dill et al, 2007;Saudemont et al, 2008;Kerner et al, 2009) and more. The prominent role of annelids in evolutionary developmental biology is now clear, and this is likely to be extended in the future.…”