Conflict reducing innovations in development enable increased multicellular complexity

Obligately multicellular organisms, where cells can only reproduce as part of the group, have evolved multiple times across the tree of life. Obligate multicellularity has only evolved when clonal groups form by cell division, rather than by cells aggregating, as clonality prevents internal conflict. Yet obligately multicellular organisms still vary greatly in ‘multicellular complexity’ (the number of cells and cell types): some comprise few cells and cell-types, and others billions of cells and thousands of types. Here, we test if variation in multicellular complexity is explained by conflict-suppressing mechanisms, namely a single cell bottleneck at the start of development, and a strict separation of germline and somatic cells. Applying a phylogenetic comparative analysis to the life-cycles 138 lineages of plants, animals, fungi and algae, we show that an early segregation of the germline stem-cell lineage is key to the evolution of more cell types. In contrast, the presence of a strict single cell bottleneck was not related to either the number of cells or cell types but was associated with early germline segregation. Our results suggest that segregating the germline earlier in development enabled greater evolutionary innovation, possibly through conflict suppression or via greater developmental flexibility.

专性多细胞生物（obligately multicellular organism）指其细胞仅能作为群体的一部分进行繁殖，这类生物已在生命之树中多次独立演化出现。专性多细胞性仅在通过细胞分裂形成克隆群体（而非细胞聚集形成群体）的情况下演化而来，因为克隆性可避免内部冲突。然而，专性多细胞生物的“多细胞复杂性”（即细胞数量与细胞类型数量）仍存在巨大差异：部分类群仅包含少量细胞与细胞类型，而另一些则拥有数十亿细胞与数千种细胞类型。本研究旨在探究多细胞复杂性的差异是否可由冲突抑制机制解释，具体为发育起始阶段的单细胞瓶颈（single cell bottleneck）以及生殖系与体细胞的严格分离。我们对植物、动物、真菌与藻类共138个类群的生命周期开展系统发育比较分析，结果显示生殖系干细胞谱系的早期分离是演化出更多细胞类型的关键。与之相反，严格单细胞瓶颈的存在与细胞数量或细胞类型数量均无关联，但与生殖系的早期分离存在相关性。本研究结果表明，在发育早期完成生殖系分离可推动更多演化创新，这一过程可能通过抑制内部冲突或提升发育灵活性实现。