Abstract
BackgroundThe polychaete annelid Capitella teleta (formerly Capitella sp. I) develops by spiral cleavage and has been the focus of several recent developmental studies aided by a fully sequenced genome. Fate mapping in polychaetes has lagged behind other spiralian taxa, because of technical limitations.ResultsTo generate a modern fate map for C. teleta, we injected 1,1'-dioctadecyl-3,3,3'3'-tetramethylindocarbocyanine perchlorate (DiI) into individual identified blastomeres through fourth-quartet micromere formation. Confocal laser scanning microscopy at single-cell resolution was used to characterize blastomere fates during larval stages. Our results corroborate previous observations from classic studies, and show a number of similarities with other spiralian fate maps, including unique and stereotypic fates for individual blastomeres, presence of four discrete body domains arising from the A, B, C and D cell quadrants, generation of anterior ectoderm from first quartet micromeres, and contributions to trunk ectoderm and ventral nerve cord by the 2d somatoblast. Of particular interest are several instances in which the C. teleta fate map deviates from other spiralian fate maps. For example, we identified four to seven distinct origins of mesoderm, all ectomesodermal. In addition, the left and right mesodermal bands arise from 3d and 3c, respectively, whereas 4d generates a small number of trunk muscle cells, the primordial germ cells and the anus. We identified a complex set of blastomere contributions to the posterior gut in C. teleta, which establishes the most complete map of posterior gut territories to date.ConclusionsOur detailed cellular descriptions reveal previously underappreciated complexity in the ontogenetic contributions to several spiralian larval tissues, including the mesoderm, nervous system and gut. The formation of the mesodermal bands by 3c and 3d is in stark contrast to other spiralians, in which 4d generates the mesodermal bands. The results of this study provide a framework for future phylogenetic comparisons and functional analyses of cell-fate specification.
Highlights
IntroductionThe polychaete annelid Capitella teleta (formerly Capitella sp. I) develops by spiral cleavage and has been the focus of several recent developmental studies aided by a fully sequenced genome
C. teleta development and fate map overview C. teleta embryos develop by unequal spiral cleavage, individual blastomeres are identifiable
The first quartet micromeres (1q) are born dexiotropically with respect to the macromeres when viewed from the animal pole; second quartet micromeres (2q) are born laeotropically, and subsequent macromere cleavages alternate between dexiotropic and laeotropic
Summary
The polychaete annelid Capitella teleta (formerly Capitella sp. I) develops by spiral cleavage and has been the focus of several recent developmental studies aided by a fully sequenced genome. Embryonic features that aid identification include differences in cell size or pigmentation, or in spindle orientation relative to the primary egg axis. Such embryos are amenable to celllineage and fate-mapping studies, which establish the developmental origins of definitive regions, tissues and organs in larval and adult animals, and provide the. A spectacular example is a group of animals that displays a pattern of early development called spiral cleavage This pattern of development is recognizable by the timing, orientation and/or size of individual cell divisions, and is found in a large number of diverse animal groups including mollusks, annelids, sipunculans, echiurans, nemerteans, myzostomids, ectoprocts, polyclad flatworms and potentially gnathostomulids. A better understanding of the exact relationships among lophotrochozoans, between members of the Platyzoa (for example, gnathostomulids, gastrotrichs, rotifers and platyhelminthes), is needed to determine whether spiral cleavage was an ancestral character for all lophotrochozoans (Spiralia) or just a subset (Trochozoa)
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