Integrative analysis of polychaete ontogeny: Cell proliferation patterns and myogenesis in trochophore larvae of Sabellaria alveolata

Abstract

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. © 2010 Wiley Periodicals, Inc.