ERK1/2 is an ancestral organising signal in spiral cleavage

Abstract

Animal development is classified as conditional or autonomous based on whether cell fates are specified through inductive signals or maternal determinants, respectively. Yet how these two major developmental modes evolved remains unclear. During spiral cleavage—a stereotypic embryogenesis ancestral to 15 invertebrate groups, including molluscs and annelids—most lineages specify cell fates conditionally, while some define the primary axial fates autonomously. To identify the mechanisms driving this change, we study Owenia fusiformis, an early-branching, conditional annelid. In Owenia, ERK1/2-mediated FGF receptor signalling specifies the endomesodermal progenitor. This cell likely acts as an organiser, inducing mesodermal and posterodorsal fates in neighbouring cells and repressing anteriorising signals. The organising role of ERK1/2 in Owenia is shared with molluscs, but not with autonomous annelids. Together, these findings suggest that conditional specification of an ERK1/2+ embryonic organiser is ancestral in spiral cleavage and was repeatedly lost in annelid lineages with autonomous development.

Annelid functional genomics reveal the origins of bilaterian life cycles

“…Fragments of chordin and Hox genes were isolated as previously described 24 using gene-specific oligonucleotides and a T7 adaptor. Riboprobes were synthesized using a T7 MEGAscript kit (ThermoFisher, AM1334) and stored at a concentration of 50 ng µl –1 in hybridization buffer at –20 °C.…”

“…Riboprobes were synthesized using a T7 MEGAscript kit (ThermoFisher, AM1334) and stored at a concentration of 50 ng µl –1 in hybridization buffer at –20 °C. Whole-mount in situ hybridization in embryonic, larval and juvenile stages were conducted as described elsewhere 24 , 26 . Antibody staining in larval stages of O. fusiformis , Magelona spp.…”

“…In particular, the larva of Oweniidae, referred to as ‘mitraria’ 12 , has an enlarged pre-oral region and a bundle of posterior chaetae, as well as a pair of nephridia and a long monociliated ciliary band similar to those of phylogenetically distant larvae of echinoderms and hemichordates 21 , 22 . Yet oweniids show many developmental characteristics that are considered ancestral to Annelida and even Spiralia as a whole 23 , 24 , including similarities in larval molecular patterns with other trochophore and bilaterian larvae 22 , 23 , 25 , 26 . Therefore, the diversity of life cycles and larval forms but generally conserved early embryogenesis and adult body plans of Annelida is an excellent model to investigate how larval traits evolve.…”

“…Therefore, O. fusiformis shows a more complete gene repertoire and ancestral syntenic chromosomal organization than other annelids. Together with its phylogenetic position and conserved early embryogenesis 23 , 24 , O. fusiformis is a key lineage to reconstruct the evolution of Annelida, and of Spiralia generally.…”

“…Moreover, anterior, trunk and posterior genes with spatially resolved expression followed different temporal dynamics in O. fusiformis , C. teleta and D. gyrociliatus . In O. fusiformis , trunk 25 and posterior 24 , 26 genes were concentrated in a small ventral area and around the anal opening of the larva and increased in spatial range and expression levels as the trunk formed (Extended Data Fig. 6g,h ).…”