Evolutionary crossroads in developmental biology: amphioxus

Abstract

SummaryThe phylogenetic position of amphioxus, together with its relatively simple and evolutionarily conserved morphology and genome structure, has led to its use as a model for studies of vertebrate evolution. In particular, the recent development of technical approaches, as well as access to the complete amphioxus genome sequence, has provided the community with tools with which to study the invertebrate-chordate to vertebrate transition. Here, we present this animal model, discussing its life cycle, the model species studied and the experimental techniques that it is amenable to. We also summarize the major findings made using amphioxus that have informed us about the evolution of vertebrate traits.Key words: Cephalochordates, Vertebrate evolution, Branchiostoma, Amphioxus, Lancelet Introduction Amphioxus (also called lancelets or cephalochordates) form one of the three chordate subphyla, along with urochordates (see Glossary, Box 1) and vertebrates (Schubert et al., 2006) (Fig. 1A). They form a small group comprising about 35 species (Poss and Boschung, 1996). The number of genera within the cephalochordate subphylum has long been debated, but recent molecular phylogenetic studies show that cephalochordates are divided into three genera (Kon et al., 2007) (Fig. 1B): Branchiostoma, Epigonichthys and Asymmetron.Described for the first time in 1774 (Pallas, 1774), lancelets were classified as molluscs and were called Limax lanceolatus. Later, in 1834, they were renamed as Branchiostoma lubricus (Costa, 1834) and classified as animals closely related to vertebrates. The first to use the name Amphioxus was William Yarrell, who named them Amphioxus lanceolatus and for the first time described their notochord (see Glossary, Box 1), the defining morphological trait of chordates (Yarrell, 1836). After these initial studies, and until the beginning of the 20th century, amphioxus was considered to be a vertebrate. A consensus was then reached whereby amphioxus were considered to be the closest living relatives of vertebrates, with urochordates representing the most basally divergent chordate lineage. These evolutionary relationships were based on morphological characteristics and on some molecular studies of rRNA genes (Winchell et al., 2002). However, in 2006, based on large molecular data set analyses, it was established that cephalochordates represent the most basally divergent lineage of chordates, being the sister group of urochordates and vertebrates (Bourlat et al., 2006; Delsuc et al., 2006) (Fig. 1A).The adult anatomy of amphioxus is vertebrate-like, but simpler. Amphioxus possess typical chordate characters, such as a dorsal hollow neural tube and notochord, a ventral gut and a perforated pharynx with gill slits, segmented axial muscles and gonads, a postanal tail, a pronephric kidney, and homologues of the thyroid gland and adenohypophysis (the endostyle and pre-oral pit, respectively) ( Fig. 2A). However, they lack typical vertebrate-specific structures, such as paired sensory organs (image-forming eye...

The evolution and conservation of left-right patterning mechanisms

“…The fourth (top) and seventh (bottom) somites are boxed in red. d, dorsal; l, left; r, right; v, ventral. Remarkably, this expression of Nodal marks the pre-somitic mesoderm, as these cells in the archenteron roof bud off to give rise to the somites shortly thereafter (Bertrand and Escriva, 2011;Holland et al, 2004;Yu et al, 2002). Concomitant with the budding off of these cells, Nodal expression becomes asymmetrical, with much stronger signals on the left than right side (Yu et al, 2002).…”

“…Because of its position at the base of the chordates, rooting the vertebrates in the phylogenetic tree (Box 1), the embryology of amphioxus has been studied in great detail (Bertrand and Escriva, 2011;Holland et al, 2004). The first asymmetry that was described concerns the alignment of the somites on the left and right sides of the notochord (Schubert et al, 2001).…”

Chordate evolution and the three-phylum system

“…B 281: 20141729 in sand. They are often called 'acraniates' in comparison with vertebrates ('craniates'), because their CNS consists of a neural tube with a small anterior vesicle that does not develop into the tri-partitioned brain seen in urochordate larvae and vertebrates [76][77][78]. Although they have no structures corresponding to well-organized eyes or a heart, as seen in vertebrates, they develop a well-organized feeding and digestive system as ciliary-mucous suspension feeders with a wheel organ, a Hatchek's pit, an endostyle and a pharynx with gill slits.…”

Novel polyclonal antibodies as a useful tool for expression studies in amphioxus embryos

“…This position has recently been affirmed especially thanks to the access to genome sequence data (Holland et al, 2008;Huang et al, 2014;Putnam et al, 2008), introduction of novel techniques (Acemel et al, 2016;Kozmikova and Kozmik, 2015;Li et al, 2017;Yue et al, 2016), and establishment of amphioxus as a model species for evolutionary developmental studies (for review see Bertrand and Escriva (2011)). Cephalochordates include three genera, namely Branchiostoma, Asymmetron and Epigonychtys.…”