The Adult Body Plan of Indirect Developing Hemichordates Develops by Adding a Hox-Patterned Trunk to an Anterior Larval Territory

Abstract

Many animals are indirect developers with distinct larval and adult body plans [1]. The molecular basis of differences between larval and adult forms is often poorly understood, adding a level of uncertainty to comparative developmental studies that use data from both indirect and direct developers. Here we compare the larval and adult body plans of an indirect developing hemichordate, Schizocardium californicum [2]. We describe the expression of 27 transcription factors with conserved roles in deuterostome ectodermal anteroposterior (AP) patterning in developing embryos, tornaria larvae, and post-metamorphic juveniles and show that the tornaria larva of S. californicum is transcriptionally similar to a truncated version of the adult. The larval ectoderm has an anterior molecular signature, while most of the trunk, defined by the expression of hox1-7, is absent. Posterior ectodermal activation of Hox is initiated in the late larva prior to metamorphosis, in preparation for the transition to the adult form, in which the AP axis converges on a molecular architecture similar to that of the direct developing hemichordate Saccoglossus kowalevskii. These results identify a molecular correlate of a major difference in body plan between hemichordate larval and adult forms and confirm the hypothesis that deuterostome larvae are "swimming heads" [3]. This will allow future comparative studies with hemichordates to take into account molecular differences caused by early life history evolution within the phylum. Additionally, comparisons with other phyla suggest that a delay in trunk development is a feature of indirect development shared across distantly related phyla.

Anteroposterior molecular registries in ectoderm of the echinus rudiment

“…Tsuchimoto and Yamaguchi () showed that the Pj‐dlx domain extends from the apical plate to the whole vestibule. Even in the indirect‐developing hemichordate Schizocardium californicum , the anterior genes, such as dlx, rx , and six3/6 , are expressed in the apical plate of larvae (Gonzalez et al, ). In our analyses, Pj‐sfrp1/5 domain was located in the apical/animal pole region (Fig.…”

“…A). Expression of gbx and en in the posterior collar ectoderm is conserved in S. californicum (Gonzalez et al, ). In P. japonica , Morino et al () indicated that Pj‐pax2/5/8 is expressed in ectoderm overlying the spine rudiments, and we confirm this (Fig.…”

Nemertean and phoronid genomes reveal lophotrochozoan evolution and the origin of bilaterian heads

“…Remarkably, Hox genes are not expressed in the proboscis and head of Notospermus nor in lophophores of Phoronis and Lingula. This anterior Hox-free region is also found in juvenile amphioxus 37 , hemichordates 38 , arthropods 39 , nemerteans 40 and annelids 41 , suggesting that the absence of Hox gene expression at the anterior end is a common adult body plan for all bilaterians.…”

Genetic Mapping and Biochemical Basis of Yellow Feather Pigmentation in Budgerigars

“…The sequence of the Schizocardium californicum polyketide synthase was provided by Chris Lowe of Hopkins Marine Station at Stanford University, and is from a previously described transcriptome assembly (Gonzalez et al, 2017). …”