Amphioxus as a Model for Mechanisms in Vertebrate Development

Abstract

For the last two centuries, the cephalochordates, commonly known as lancelets or amphioxus, have been central to investigate the evolutionary genesis of vertebrates. At first, by classical morphologists fascinated by their odd but at the same time familiar anatomical traits and later by molecular biologists giving the first insights into their slow evolving nature. The present data available not only holds amphioxus as an organism of preternatural importance within the tree of life but also boosts its potential to untangle the molecular basis underlying the vertebrate complexity. This is a walk through the past and present of the amphioxus field merging morphological and molecular data in linkage with the fossil record and the modern vertebrates. The resulting picture is drawn together with comparative maps of genome organisation, gastrulation and the origin of the vertebrate organiser, neurulation and the origin of the neural crest, and shared signalling mechanisms between vertebrates and amphioxus during development. Special attention is also given to some of the most critical vertebrate novelties and how the pre‐duplicative amphioxus genetic toolkit might have contributed to set the basis for evolving complexity in the course of vertebrate evolution. Key Concepts: Cephalochordates occupy at present the key phylogenetic position to get insights into the invertebrate–vertebrate transition and the evolutionary genesis of vertebrates. Whole‐genome duplications in the lineage leading to modern vertebrates might have established the basis for molecular and morphological innovation. The amphioxus genome appears to be the best surrogate available for the ancestral chordate genome regarding the gene content, gene structure and chromosomal organisation. The amphioxus prototypical body plan with respect to vertebrates facilitates the comparative analysis and linkage between invertebrates and vertebrates. The pre‐duplicative genome of amphioxus offers the possibility of analysing vertebrate‐like gene regulatory networks in a simpler biological context with a reduced number of molecular players.

Restricted proliferation during neurogenesis contributes to regionalization of the amphioxus nervous system

“…The central nervous system (CNS) of amphioxus has been the subject of intense study. This is due to the key phylogenetic position of amphioxus (cephalochordate) as the sister group to all other chordates, which makes them unique to investigate the evolutionary origin of vertebrate nervous systems (Garcia-Fernàndez and Benito-Gutiérrez, 2009; Benito-Gutiérrez, 2011; Holland, 2016; Holland and Holland, 2021). These studies have primarily employed two distinct approaches: first, through exquisitely detailed morphological descriptions of the late amphioxus larva and adult brain anatomy by electron microscopy (Lacalli et al, 1994; Lacalli, 1996; Wicht and Lacalli, 2005); and second, through molecular characterization of cell types, via analysis of gene expression patterns and protein localization in the CNS during embryogenesis and in adult amphioxus (Benito-Gutiérrez, 2006; Yu et al, 2007; Albuixech-Crespo et al, 2017; Holland, 2017).…”

Restricted Proliferation During Neurogenesis Contributes to Regionalisation of the Amphioxus Nervous System

“…Whilst is generally agreed that vertebrate nervous systems are very similar at early developmental stages and probably built up on a same common ground plan, little is known about the mechanisms that makes them architecturally so different later in development ( Nieuwenhuys, 2017 ). Central to this question is understanding the principles governing the establishment of the nervous system “bauplan” (or ground plan), common to all invertebrate and vertebrate chordates, for which amphioxus is ideally placed given its key phylogenetic position, branching at the root of the chordate tree ( Garcia-Fernàndez and Benito-Gutiérrez, 2009 ; Benito-Gutiérrez, 2011 ; Holland, 2016 ; Holland and Holland, 2021 ).…”