Evolution of multicellularity and reproductive strategies in yellow-green algae (Xanthophyceae, Heterokontophyta)

Abstract

The evolution of multicellularity has long been linked to reproductive strategies. A long-standing debate concerns whether multicellular organisms are primarily stabilized by small single-cell propagules that minimize genetic heterogeneity or by larger multicellular and multinucleate propagules that may improve developmental success and survival of individuals. the Xanthophyceae provides an excellent model for investigating these questions, exhibiting transitions between unicellular to multicellular filamentous and coenocytic forms together with diverse reproductive modes, including single-cell zoospores and autospores, and multinucleate monospores and akinetes. However, a robust phylogenetic framework and systematic analyses of character evolution have remained lacking in this lineage. Here, we present a phylogenomic framework based on a nuclear dataset of 680 genes from 18 species, including 17 newly generated transcriptomes. Nuclear phylogenies robustly resolve all sampled inter-ordinal and inter-familial relationships with full concordance between concatenation and coalescent analyses, while plastid (141 genes) and mitochondrial (31 genes) datasets from 33 species recover identical topologies. Based on these results, we establish one new order (Pseudopleurochloridales), emend one order (Heterococcales), and propose five new families. Ancestral character reconstruction indicates at least four independent transitions from unicellular ancestors to simple multicellularity. Bayesian analyses of multicellularity and reproductive characters show that these transitions were consistently accompanied by shifts from multiple autospore-type propagules toward single monospore- and akinete-type propagules, whereas reversions to unicellularity were associated with the reappearance of autospore-based reproduction. These results provide a phylogenomic framework for understanding multicellular evolution in Xanthophyceae and shed light on the relationship between reproductive modes and the emergence of simple multicellularity.