Evolutionary and developmental transcriptomics in brown algae

Complex multicellularity has emerged independently multiple times across the eukaryotic tree of life. A longstanding question remains whether the repeated emergence of this trait reflects shared evolutionary constraints or lineage-specific contingencies. Brown algae, a stramenopile lineage, present a valuable comparative system to address this question, due to their independent evolution of complex multicellularity. This thesis applies evolutionary transcriptomics alongside genomic and epigenomic approaches to investigate the origin and diversification of complex multicellularity, focusing on brown algae. To this end, I contributed to GenEra, a bioinformatic software for inferring gene family founder events (‘gene age’) from taxonomically-resolved outputs of the pairwise sequence aligner DIAMONDv2. Gene age inference across animals, plants and fungi uncovered bursts of gene family origination that coincide with macro-evolutionary transitions such as the origin of complex multicellularity. By coupling gene age inference with developmental transcriptome profiling, I show that brown algal embryogenesis follows a transcriptomic hourglass pattern, with maximal conservation during mid-embryogenesis. Notably, this pattern mirrors observations in animals and plants, showing that embryogenesis is subject to shared constraints that recur across independently evolved complex multicellular lineages. More generally, however, brown algal transcriptomes evolve particularly rapidly, potentially facilitating the remarkable diversification of morphological and sexual characteristics within this clade. This rapid transcriptome evolution may be facilitated by a distinct brown algal genome regulatory system, characterised by new regulatory motifs and repurposing of H3K79me2 into a repression-associated mark, as well as loss of Polycomb Repressive Complex subunits and DNA methylation. Taken together, these results, enabled through my contributions to methods in evolutionary genomics and transcriptomics, expand the potential genomic regulatory foundation or ‘starting points’ from which multicellularity can emerge and diversify. Yet, despite this diversity, similar patterns of transcriptome evolution play out across independently-evolving lineages. These results suggest that complex multicellularity itself may bias its own future evolutionary trajectory.