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Evolution and development in Spiralia: Early progeny of the mesodermal lineage in the leech Helobdella sp. (Austin)


One of the major questions in evolutionary biology is, how changes in development over time result in diversity of adult body plans. Spiralia are a highly diverse group of protostome taxa, in terms of their adult body plans, but which nonetheless share a highly conserved pattern of early cell divisions, called spiral cleavage. Thus, in the early embryos of spiralian taxa, homologous blastomeres are identifiable on the basis of their embryonic origins and their subsequent fates in later development. One of the best-known examples of such homologous blastomeres are the precursors of left and right mesoderm, which arise from the bilateral division of a cell classically known as micromere 4d. Given the dramatic differences among body plans of various spiralian species (consider the mesoderm of an unsegmented mollusk and that of a segmented annelid, such as the leech, for example), it is obvious that the 4d lineages must diverge at some point in development of different species.

In the leech Helobdella, a clitellate annelid, the homolog of the cell 4d is called DM" and its bilateral division gives rise to two large stem cells (M teloblasts) whose iterated divisions yield precursors (m blast cells) of segmental mesoderm. In this work I present new plasmid driven high-resolution cell lineage tracing techniques. Using high-resolution tracers in conjunction with standard tracers, I have been able to study the early progeny of the M teloblasts in great detail. I have found that each M teloblast produces six precursors of non-segmental mesoderm, prior to initiating the production of purely segmental blast cells. While all segmental blast cells undergo identical stereotyped early divisions and give rise to homologous definitive pattern elements, the early clonal distributions of the first six cells, as well as their definitive contributions differ from each other and from the segmental blast cells. The early mesodermal progeny make major contributions to anterior non-segmental mesoderm especially throughout the head and the muscular proboscis, an eversible, specialized feeding apparatus.

Collaborative work with Ayaki Nakamoto on more detailed analysis of the 4d lineage in the oligochaete Tubifex revealed that, in this annelid too, the 4d lineage makes contributions to anterior non-segmental mesoderm. However, unlike Helobdella, Tubifex ingest sediments and are filter feeders, and thus have different head and foregut morphology. In accord with these differences, I find that the anterior contributions of the M lineage differ between these two annelids. These differences illustrate that the 4d lineage exhibits evolutionary plasticity and that potentially small changes in the developmental program of the M teloblasts can result in a diversity of adult body plans.

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