Diversification of habenular organization and asymmetries in teleosts: Insights from the Atlantic salmon and European eel

Abstract

Habenulae asymmetries are widespread across vertebrates and analyses in zebrafish, the reference model organism for this process, have provided insight into their molecular nature, their mechanisms of formation and their important roles in the integration of environmental and internal cues with a variety of organismal adaptive responses. However, the generality of the characteristics identified in this species remains an open question, even on a relatively short evolutionary scale, in teleosts. To address this question, we have characterized the broad organization of habenulae in the Atlantic salmon and quantified the asymmetries in each of the identified subdomains. Our results show that a highly conserved partitioning into a dorsal and a ventral component is retained in the Atlantic salmon and that asymmetries are mainly observed in the former as in zebrafish. A remarkable difference is that a prominent left-restricted pax6 positive nucleus is observed in the Atlantic salmon, but undetectable in zebrafish. This nucleus is not observed outside teleosts, and harbors a complex presence/absence pattern in this group, retaining its location and cytoarchitectonic organization in an elopomorph, the European eel. These findings suggest an ancient origin and high evolvability of this trait in the taxon. Taken together, our data raise novel questions about the variability of asymmetries across teleosts and their biological significance depending on ecological contexts.

Analysis of a shark reveals ancient, Wnt dependent, habenular asymmetries in jawed vertebrates

“…In support of this interpretation, the phylogenetic distribution of asymmetries, shared by chondrichthyans and members of the dipneusts and polypterids, respectively outgroups to tetrapods within sarcopterygians and to neopterygians within the actinopterygians, does not evoke a punctuated presence/absence pattern, as observed for instance for the left-restricted nucleus recently identified in teleosts 16 . Furthermore, the relative organization of habenular territories appears very similar in the mouse and the frog on the one hand, and within teleosts and in the spotted gar on the other hand 16 , arguing against a rapid drift of the corresponding molecular architectures in these taxa. Concerning the two tetrapods, it is intriguing that in the mouse, several orthologues of catshark Right-LHb markers ( Prox1 , Rorα , and Rerg ) are not expressed in the habenulae but rather in the adjacent paraventricular nucleus of thalamus 31 .…”

“…While we cannot completely rule out convergent evolution processes to explain the similarities observed between chondrichthyans, dipneusts and polypterids, we favour an alternative, more parsimonious hypothesis, and propose that the asymmetry pattern observed in the catshark lateral habenulae reflects an ancestral trait of jawed vertebrates, independently lost in tetrapods and neopterygians (Fig.8a). In support of this conclusion, the phylogenetic distribution of asymmetries, shared by members of chondrichthyans and of dipneusts and polypterids, respectively outgroups to tetrapods and neopterygians in sarcopterygians and actinopterygians, is very different from, for instance, the punctuated presence/absence pattern of another asymmetric trait recently identified in teleosts 16 . Furthermore, the relative organization of the territories identified appears very similar between the mouse and xenopus on the one hand and within teleosts on the other hand, arguing against a rapid drift of the corresponding molecular architecture in these taxa.…”

“…8a). In support of this conclusion, the phylogenetic distribution of asymmetries, shared by members of chondrichthyans and of dipneusts and polypterids, respectively outgroups to tetrapods and neopterygians in sarcopterygians and actinopterygians, is very different from, for instance, the punctuated presence/absence pattern of another asymmetric trait recently identified in teleosts 16 .…”

“…Morphological characterizations suggest that they considerably vary in nature and degree across vertebrates (size, cellular or nuclei organisation, connectivity pattern) 10 . In line with this complexity, more detailed molecular characterizations, essentially focused on teleosts thus far, highlight complex presence/absence patterns of asymmetric traits, suggestive of a rapid drift in this taxon 16,17 . However, whether habenular asymmetries in teleosts reflect the vertebrate or gnathostome ancestral state is unclear, since they may employ highly divergent mechanisms for their formation 18 .…”