Evolution of a Metamorphic Life Cycle in a Marine Invertebrate: Origin of the Pilidium Larva in the Phylum Nemertea
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The pilidium is a novel larval form that arose within a single clade in the phylum Nemertea - the Pilidiophora. While the sister clade of the Pilidiophora, Hoplonemertea, and the basal nemertean clade develop relatively directly, pilidiophorans have a long- lived feeding larva with a body plan distinctly different from that of the juvenile. Uniquely, the pilidiophoran juvenile develops inside the larva from several discrete rudiments. The purpose of this dissertation is to illuminate how this life cycle evolved, both the developmental-genetic mechanisms and timing with respect to the three nemertean clades. With colleagues I describe development of the hoplonemertean Pantinonemertes californiensis using confocal microscopy. We find that the larva possesses two pairs of epidermal invaginations and a transitory epidermis. We hypothesize that these features are homologous to invaginated rudiments and loss of larval epidermis in pilidial development. We examine the expression of the Hox genes during development of the pilidiophoran Micrura alaskensis. We identify nine Hox genes and one ParaHox gene with transcriptome analysis and molecular cloning and determine their developmental expression patterns. We find that Hox genes are not expressed in the pilidium at any stage. Instead, Hox gene expression is restricted to the juvenile trunk rudiments, suggesting that the larva and juvenile are patterned with somewhat dissociated mechanisms. We examine developmental genes in P. californiensis. We find that Hox genes are expressed in the posterior invaginations. We find Six3/6 expression in both pilidial cephalic discs and the hoplonemertean anterior invaginations. Our results support the homology between the pilidium imaginal discs and hoplonemertean larval invaginations. This finding, which is also supported by cell-proliferation patterns, suggests that invaginated rudiments evolved before the pilidiophorans diverged from the hoplonemerteans. Juvenile growth via invaginated rudiments may have paved the way for the more complete separation between larval and juvenile morphogenesis seen in modern pilidiophorans. These discoveries illuminate how larval and juvenile bodies can become mechanistically and morphogenetically dissociated, allowing for somewhat independent evolution across life stages. This may help explain the evolution of metamorphosis and the evolution of the great diversity of marine invertebrate larval forms. This dissertation includes published and unpublished co-authored material.