Comparative development of spiralian larvae

Abstract

Bryozoans and brachiopods are sessile, mostly marine animals, that use an elegant crown of tentacles for filter-feeding. They are related to molluscs, segmented worms and other animals in a outstandingly diverse group of invertebrates named Spiralia. Most spiralians show a conserved pattern of embryonic development—spiral cleavage—but bryozoans and brachiopods deviate from their relatives. To better understand the developmental diversity and evolution of spiralian development, I examine bryozoan and brachiopod embryogenesis and larval morphology in comparison to other spiralians. Some bryozoans develop through a unique stereotypic cleavage with biradial symmetry, and lack spiral cleavage. Here I describe the first detailed cell lineage of the bryozoan Membranipora membranacea by tracing the fate of embryonic blastomeres from the egg until the larval stage. I further investigate the molecular patterning of the larvae by analysing the expression of conserved developmental genes. Our data reveals several similarities between the fate map and gene expression of M. membranacea and the typical spiral-cleaving embryos, despite the loss of the spiral symmetry. The cell lineage resemblance might be a direct modification of the spiral cleavage pattern, or alternatively, be an evolutionary convergence that reflects a conserved underlying molecular patterning of the embryos. Adult brachiopods do not have a segmented body, but their larvae have body boundaries that resemble annelid segments. To test whether genes involved in the patterning of segment boundaries also pattern brachiopod larval boundaries, I characterize the expression of the segment polarity genes engrailed, wnt1 and hedgehog during the development of the brachiopods T. transversa and N. anomala. I found that engrailed is the only gene consistently demarcating the embryonic head/trunk boundary in the larvae of both species. Surprisingly, the gene expression profile at this brachiopod boundary is more similar to a boundary in the vertebrate brain than to segment boundaries. Our data suggests that the ancestral expression of engrailed was nonsegmental in the trunk ectoderm, and might have been independently recruited to the segment boundaries of annelids and arthropods. This work provides basic embryological information, combining cell lineage tracing with morphological and molecular data for two understudied spiralian taxa, bryozoans and brachiopods. These comparative data bring insights to the evolution of two major morphological traits, spiral cleavage and segmentation, and to the evolution of the great diversity of spiralian larval forms.