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Aspects of muscle development are still widely neglected in studies on invertebrate ontogeny, which is probably at least partly due to the inherent complexity of animal myoanatomical bodyplans. This has resulted in significant gaps in our understanding of the evolutionary and ontogenetic origin of this crucial mesoderm-derived organ system, particularly in indirect developing representatives of the Lophotrochozoa. Here, we document the temporal and spatial patterns of muscle formation and cell proliferation in the polychaete Sabellaria alveolata during planktotrophic larval development in order to assess the presumed generation of muscle units and segments from a posterior growth zone. In addition, we address the question whether the three primary segments differ in their mode of myogenesis from the subsequently forming segments. We found that in the first three segments the ventral transverse muscles differentiate from anterior to posterior, whereas the ventral oblique muscles develop simultaneously. Hence, subsequent and simultaneous developmental processes of specific muscle groups are possibly regulated in different ways, thus emphasizing the plasticity of the formation of metamerically arranged organ systems in polychaetes. The occurrence of three clusters of proliferating cells in the trunk region of the metatrochophore indicates synchronous subdivision of the larval mesoderm in the first three segments. Assuming a polychaete-like ancestor at the base of the annelid tree, comparative analysis suggests that the bodywall of the last common annelid ancestor might have been devoid of circular muscles and consisted of four separate longitudinal muscle strands that develop from anterior to posterior.

The embryos of indirect developers generate an intermediate larval stage that nourishes the proliferation of undifferentiated multipotent cell precursors in charge of postembryonic adult formation. Multipotency affects the regulation of many genes and seems to be mediated in part by chromatin modification. Chromatin transcriptional properties are regulated by histone modification and by incorporation of peculiar histone variants. The histone variant H2A.Z is associated with transcriptionally competent chromatin and silent genes primed for activation or permanent repression. However, despite the extensive mechanistic characterizations in unicellular eukaryotes, the essential role of the highly conserved H2A.Z variant during animal embryogenesis remains obscure. We show that the expression of H2A.Z in the larvae of two distant indirectly developing marine invertebrates, a polychaete and a sea urchin, remains high in all their embryonic and postembryonic developmentally competent cell precursors, and declines during their differentiation. In particular, the expression in undifferentiated multipotent adult precursors during feeding larval stages in both organisms provides unique insight about its general association with developmental potential. Our experiments confirm previous reports indicating that the expression of H2A.Z is proliferation (DNA synthesis) independent, in contrast with the DNA synthesis dependence of "mainstream" histones. We suggest that similar H2A.Z transcriptional functions previously identified in unicellular organisms also help to maintain an open chromatin state competent for transcriptional-regulatory transactions during metazoan development.

In order to address the question of the conservation of posterior growth mechanisms in bilaterians, we have studied the expression patterns of the orthologues of the genes caudal, even-skipped, and brachyury in the annelid Platynereis dumerilii. Annelids belong to the still poorly studied third large branch of the bilaterians, the lophotrochozoans, and have anatomic and developmental characteristics, such as a segmented body plan, indirect development through a microscopic ciliated larva, and building of the trunk through posterior addition, which are all hypothesized by some authors (including us) to be present already in Urbilateria, the last common ancestor of bilaterians. All three genes are shown to be likely involved in the building of the anteroposterior axis around the slit-like amphistomous blastopore as well as in the patterning of the terminal anus-bearing piece of the body (the pygidium). In addition, caudal and even-skipped are likely involved in the posterior addition of segments. Together with the emerging results on the conservation of segmentation genes, these results reinforce the hypothesis that Urbilateria had a segmented trunk developing through posterior addition.