Inferring the intrinsic and extrinsic drivers of species diversification and phenotypic disparity across the tree of life is a major challenge in evolutionary biology. In green plants, polyploidy (or whole-genome duplication, WGD) is known to play a major role in microevolution and speciation, but the extent to which WGD has shaped macroevolutionary patterns of diversification and phenotypic innovation across plant phylogeny remains an open question. Here, we examine the relationship of various facets of genomic evolution—including gene and genome duplication, genome size, and chromosome number—with macroevolutionary patterns of phenotypic innovation, species diversification, and climatic occupancy in gymnosperms. We show that genomic changes, such as WGD and genome-size shifts, underlie the origins of most major extant gymnosperm clades, and notably, our results support an ancestral WGD in the gymnosperm lineage. Spikes of gene duplication typically coincide with major spikes of phenotypic innovation, while increased rates of phenotypic evolution are typically found at nodes with high gene-tree conflict, representing historic population-level dynamics during speciation. Most shifts in gymnosperm diversification since the rise of angiosperms are decoupled from putative WGDs and instead are associated with increased rates of climatic occupancy evolution, particularly in cooler and/or more arid climatic conditions, suggesting that ecological opportunity, especially in the later Cenozoic, and environmental heterogeneity have driven a resurgence of gymnosperm diversification. Our study provides critical insight on the processes underlying diversification and phenotypic evolution in gymnosperms, with important broader implications for the major drivers of both micro- and macroevolution in plants.

推断生命树中物种多样化和表型差异的内在和外在驱动因素是进化生物学的一个主要挑战。在绿色植物中，多倍体（或全基因组复制，WGD）已知在微观进化和物种形成中起着重要作用，但 WGD 在多大程度上塑造了植物系统发育中多样化和表型创新的宏观进化模式仍然是一个悬而未决的问题。在这里，我们研究了基因组进化的各个方面（包括基因和基因组复制、基因组大小和染色体数量）与表型创新、物种多样化和裸子植物气候占据的宏观进化模式之间的关系。我们表明基因组变化，例如 WGD 和基因组大小的变化，是现存大多数主要裸子植物进化枝起源的基础，值得注意的是，我们的结果支持裸子植物谱系中的祖先 WGD。基因复制的峰值通常与表型创新的主要峰值同时发生，而表型进化率的增加通常出现在基因树冲突高的节点，代表物种形成过程中的历史种群水平动态。自被子植物兴起以来，裸子植物多样化的大部分变化都与假定的 WGD 脱钩，而是与气候占用率的增加有关，特别是在凉爽和/或更干旱的气候条件下，这表明生态机会，特别是在新生代晚期，和环境异质性推动了裸子植物多样化的复兴。