The characterization of larval homology: transcriptomic insights into the origin and evolution of animal life cycles

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The majority of animals have a complex biphasic life cycle characterized by distinctive larval and adult body plans. Since the 1800s, the origins of marine larvae have puzzled embryologists, resulting in a long and convoluted history of theoretical literature, which largely focus on two central questions: (1) are extant larvae or adults more representative of the ancestral animal body plan, and (2) how many times did marine larvae evolve across metazoan phyla. Despite the ecological and developmental importance of this developmental mode, there is still no concrete evidence for when or how the biphasic life cycle evolved. However, recent studies predict that biphasy is an ancient synapomorphic trait of all metazoans, suggesting that ontogenies divided into distinct larval and adult phases represent the ancestral animal state. Therefore larval body plans are likely to be homologous in most animal phyla. In the present age of genomic data, these speculative theories have yet to be proven or refuted by empirical evidence. Therefore, in the present study, I employ novel computational methodology to re-examine established conceptual frameworks for life cycle evolution to create a unified model for animal body plan evolution. Here, I use the basal marine sponge, Amphimedon queenslandica, as a foundational case study for life cycle evolution. Because the majority of bioinformatic tools were developed in and optimized for classic vertebrate model systems, I first evaluate the validity of computational methods for functional gene characterization in an early branching non-model system. I find that functional characterization methods such as gene ontology (GO) are overly-specific and largely variable between annotation methods, and propose a new pipeline to effectively extract biological meaning from a non-model ontogeny. Using these tools, I characterize the pelagobenthic transition from free-swimming larvae to sessile adults in A. queenslandica. I find that larval and adult transcriptomes largely employ a shared transcriptional toolkit that is primarily composed of ancient pre-metazoan genes. However, I also find evidence for phase-specific regulatory modules characterized by the unequal distribution of gene age. Specifically, I show that the larval transcriptome is enriched in older, pre-metazoan genes, while the adult transcriptome is largely composed of novel, lineage specific innovations. To place these findings from A. queenslandica in an evolutionary context, I acquired comparable datasets from five other biphasic metazoan lineages across the animal tree including: the coral, Acropora digitifera, the mollusc, Haliotis asinina, the hemichordate, Balanoglossus misakiensis, the sea urchin, Strongylocentrotus purpuratus, and the ascidian, Herdmania momus. Through this comparative approach, I find that the majority of the genes that are significantly differentially expressed during metamorphosis are lineage-specific innovations. However, many of these co-expressed, taxonomically restricted genes appear to be regulated by conserved transcription factors in multiple species. Taken together, these findings provide the first genomically informed framework for the origins of animal biphasy. Here I discuss the implications of these results in light of historical hypotheses for larval evolution, and propose a novel conceptual framework for animal life cycle evolution.