Ancestry of motor innervation to pectoral fin and forelimb

Abstract

Motor innervation to the tetrapod forelimb and fish pectoral fin is assumed to share a conserved spinal cord origin, despite major structural and functional innovations of the appendage during the vertebrate water-to-land transition. In this paper, we present anatomical and embryological evidence showing that pectoral motoneurons also originate in the hindbrain among ray-finned fish. New and previous data for lobe-finned fish, a group that includes tetrapods, and more basal cartilaginous fish showed pectoral innervation that was consistent with a hindbrain-spinal origin of motoneurons. Together, these findings support a hindbrain–spinal phenotype as the ancestral vertebrate condition that originated as a postural adaptation for pectoral control of head orientation. A phylogenetic analysis indicated that Hox gene modules were shared in fish and tetrapod pectoral systems. We propose that evolutionary shifts in Hox gene expression along the body axis provided a transcriptional mechanism allowing eventual decoupling of pectoral motoneurons from the hindbrain much like their target appendage gained independence from the head.

Tetrapod-like axial regionalization in an early ray-finned fish

“…In zebrafish, both the HoxC3 marker for tetrapod forelimb position and Hox4 marker for tetrapod cervical -thoracic transition are expressed behind the pectoral fin origin [1,16,18]. If an elongated, Hox-defined cervical region is ancestral for vertebrates, then it would be likely that the shoulder girdle simply moved relative to this series during tetrapod evolution, rather than becoming separated from the skull through axial elongation [15,16,22]. However, it is important to note that all the above interpretations depend on the assumption that the same general Hox domains related to specific vertebral regions in all vertebrates.…”

“…Even the origin of the tetrapod body plan has been linked to clade-specific elongation of the trunk and related changes in the placement of nested Hox expression domains [9,13,14]. The process was capped by the appearance of a flexible, distinct neck (cervical region) and the evolution of a distinct sacrum in early tetrapods and their relatives [13][14][15][16][17]. Regional distinctions, many involving reinforcement of the axial column, arose in multiple tetrapod lineages from the Devonian (416-359 Ma) onwards and are widely considered to be an adaptation to terrestrial lifestyles [14].…”

Zebrafish foxc1a drives appendage-specific neural circuit development

“…Importantly, fin muscle innervation is highly stereotyped (Ma et al, 2010;Thorsen and Hale, 2007), providing an excellent model system with which to determine whether the convergence of spinal motor nerves at the plexus is a prerequisite for proper fin innervation and function, and to identify key players selectively required for the development of the neural circuitry critical for the mobility of vertebrate appendages. Using a combination of forward genetics and whole-genome sequence analysis, we first report on a mutant we isolated in a forward genetic screen based on aberrant projections of fin-innervating motor nerves, and we demonstrate that this mutant phenotype is caused by a presumptive null mutation in the foxc1a transcription factor.…”

A conserved axon type hierarchy governing peripheral nerve assembly

“…We next asked whether the apparently conserved role of MEs in establishing trunk SA trajectories would similarly govern assembly of peripheral nerve pathways that co-evolved with the tetrapod limb (Butler and Hodos, 2005;Luria et al, 2008;Ma et al, 2010). Similar to zebrafish, genetic ablation of motor neurons or their progenitors prior to ME extension in chick and mouse (supplementary material Figs S2G,H and S3A-J) resulted in markedly reduced SA extension rates ( Fig.…”