Abstract

BackgroundDuring embryonic development of segmented animals, body segments are thought to arise from the so-called "posterior growth zone" and the occurrence of this "zone" has been used to support the homology of segmentation between arthropods, annelids, and vertebrates. However, the term "posterior growth zone" is used ambiguously in the literature, mostly referring to a region of increased proliferation at the posterior end of the embryo. To determine whether such a localised posterior proliferation zone is an ancestral feature of Panarthropoda (Onychophora + Tardigrada + Arthropoda), we examined cell division patterns in embryos of Onychophora.ResultsUsing in vivo incorporation of the DNA replication marker BrdU (5-bromo-2'-deoxyuridine) and anti-phospho-histone H3 immunolabelling, we found that a localised posterior region of proliferating cells does not occur at any developmental stage in onychophoran embryos. This contrasts with a localised pattern of cell divisions at the posterior end of annelid embryos, which we used as a positive control. Based on our data, we present a mathematical model, which challenges the paradigm that a localised posterior proliferation zone is necessary for segment patterning in short germ developing arthropods.ConclusionsOur findings suggest that a posterior proliferation zone was absent in the last common ancestor of Onychophora and Arthropoda. By comparing our data from Onychophora with those from annelids, arthropods, and chordates, we suggest that the occurrence of a "posterior growth zone" currently cannot be used to support the homology of segmentation between these three animal groups.

Highlights

  • During embryonic development of segmented animals, body segments are thought to arise from the so-called “posterior growth zone” and the occurrence of this “zone” has been used to support the homology of segmentation between arthropods, annelids, and vertebrates

  • To obtain comparative data from Onychophora, we applied the anti-BrdU immunolabelling in elongating embryos of the velvet worm species Euperipatoides rowelli

  • We did not detect a higher number of BrdU labelled cells at the posterior end of the onychophoran embryos than in the rest of the body (Figures 1A-C)

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Summary

Introduction

During embryonic development of segmented animals, body segments are thought to arise from the so-called “posterior growth zone” and the occurrence of this “zone” has been used to support the homology of segmentation between arthropods, annelids, and vertebrates. The term “posterior growth zone” is used ambiguously in the literature, mostly referring to a region of increased proliferation at the posterior end of the embryo. Segments are commonly believed to originate from the so-called “posterior growth zone” (review [1]). This term has been applied very broadly in the past, which has resulted in ambiguity. A “posterior growth zone” is lacking completely from embryos of urochordates [1], as evidenced by various cell lineage and cell proliferation studies [27,28,29]

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