Cell-cell interactions in dorsoventral patterning of the segmental ectoderm of the leech Helobdella robusta: differences between the rostral and midbody segments of the same individual and variation among geographical strains

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2004

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Kuo, Dian-han

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Developmental origins and the cell lineage patterns of segmental ectoderm are evolutionary conserved in clitellate annelids. Recent comparative studies have shown that developmental pathways can be highly variable even if their morphological end product is evolutionarily conserved. To see whether this kind of evolutionary dissociation can be applied to segmentally homologous ‘modules’ in the same individuals, I compared axial patterning pathways in different segments of the leech Helobdella robusta. Distinct cell lineage origins of homologous O and P pattern elements in the ectoderm of the rostral segments and the midbody segments were previously revealed by lineage tracer injection experiments. In the rostral segments, these pattern elements arise from a single OP lineage. In the midbody segments, these pattern elements arise from separated O and Plineages. In the leech, the O and P lineages of the midbody are the members of the O/P equivalence group and are conditionally specified by cell-cell interactions. Ablation experiments revealed that the cell-cell interactions involved in the development of the OP lineage are different from those in the O/P equivalence group, despite the morphological similarity of their descendant tissues. These data suggest that serially homologous structures in different segments of the same individual can develop via distinct developmental pathways. To further explore the dissociability of developmental pathway and its morphological outcome in an evolutionary context, symmetry-breaking pathways in the O/P equivalence group of the midbody segments were compared in three closely-related laboratory strains of Helobdella. It was found that the mesoderm, the M lineage, and the dorsal ectoderm, the Q lineage, are redundantly involved in symmetry breaking of the O/P equivalence group in one particular leech strain, while the Q lineage is both necessary and sufficient for symmetry breaking of the O/P equivalence group in a second strain. Results from this comparative study of the symmetry breaking pathways in closely related leech strains suggest that redundancy may play an important role in the evolution of developmental pathways. Additional evolutionary implications of these findings will be discussed.

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