Molecular regionalization of the developing amphioxus neural tube challenges major partitions of the vertebrate brain

Abstract

All vertebrate brains develop following a common Bauplan defined by anteroposterior (AP) and dorsoventral (DV) subdivisions, characterized by largely conserved differential expression of gene markers. However, it is still unclear how this Bauplan originated during evolution. We studied the relative expression of 48 genes with key roles in vertebrate neural patterning in a representative amphioxus embryonic stage. Unlike nonchordates, amphioxus develops its central nervous system (CNS) from a neural plate that is homologous to that of vertebrates, allowing direct topological comparisons. The resulting genoarchitectonic model revealed that the amphioxus incipient neural tube is unexpectedly complex, consisting of several AP and DV molecular partitions. Strikingly, comparison with vertebrates indicates that the vertebrate thalamus, pretectum, and midbrain domains jointly correspond to a single amphioxus region, which we termed Di-Mesencephalic primordium (DiMes). This suggests that these domains have a common developmental and evolutionary origin, as supported by functional experiments manipulating secondary organizers in zebrafish and mice.

Amphioxus photoreceptors - insights into the evolution of vertebrate opsins, vision and circadian rhythmicity

“…This improved circuitry can be found in adult lamprey and jawed vertebrates, where the signal is transmitted to a tectum, localized in a mesencephalic region defined by Pax2 and Engrailed expression. New data, however, show that the amphioxus CV exhibits characteristics typical of both diencephalon and mesencephalon without clear distinguishable borders (Albuixech-Crespo et al, 2017). This would also be supported by the proposed visual circuitry in amphioxus, where the projecting Row2 neurons send their processes to the Di-Mesencephalic part of CV.…”

“…Despite the difficulties in defining homology between amphioxus CV and vertebrate brain (Albuixech-Crespo et al, 2017), the homology between FE and vertebrate eyes appears simpler. Amphioxus orthologues of transcription factors important for development of vertebrate retinal neurons and retinal pigmented epithelium (RPE) were found to be expressed in the developing FE (Vopalensky et al, 2012).…”

“…Based on morphological and molecular analysis, the cerebral vesicle is considered to be a homolog of the vertebrate diencephalon or di-plus mesencephalon with indistinguishable borders (Albuixech-Crespo et al, 2017;Holland, 2017). Amphioxus possesses four distinct photoreceptive organs -the frontal eye (FE), lamellar body (LB), Joseph cells (JCs) and dorsal ocelli (DO) (Fig.…”

Gaskell revisited: new insights into spinal autonomics necessitate a revised motor neuron nomenclature

“…Peripherally, the molecular basis for branchial slit formation apparently is conserved with hemichordates (Lowe, et al, 2015, Simakov, et al, 2015) and, like the central nervous system patterning (Albuixech-Crespo, et al, 2017), is thus likely ancestral for deuterostomes. This strongly suggests that BMs and the transcription factors driving their specification evolved in the prechordate bilaterian lineage, and already in cephalochordates and urochordates were utilized specifically to innervate branchial musculature (Dufour, Chettouh, Deyts, De Rosa, Goridis, Joly and Brunet, 2006, Fritzsch and Northcutt, 1993a).…”

Field Homology: Still a Meaningless Concept

“…The line that separates when a character exists, and when it does not, disappears. It has been suggested, for example, that all vertebrate embryos possess exactly the same set of developmental fields in an invariant organizational Bauplan [Albuixech-Crespo et al, 2017]. The rather alarming implication is that every part of the nervous system in every vertebrate can be said to possess a homolog in every other vertebrate, that everything was present since the beginning of the vertebrates or earlier, and that there can be nothing new in brain evolution.…”