Department of Science and Education, Negaunee Integrative Research Center, The Field Museum, Chicago, IL 60605;
Botanischer Garten und Botanisches Museum, Freie Universität Berlin, 14195 Berlin, Germany.
Proc Natl Acad Sci U S A. 2020 Sep 1;117(35):21495-21503. doi: 10.1073/pnas.2001913117. Epub 2020 Aug 13.
Symbioses are evolutionarily pervasive and play fundamental roles in structuring ecosystems, yet our understanding of their macroevolutionary origins, persistence, and consequences is incomplete. We traced the macroevolutionary history of symbiotic and phenotypic diversification in an iconic symbiosis, lichens. By inferring the most comprehensive time-scaled phylogeny of lichen-forming fungi (LFF) to date (over 3,300 species), we identified shifts among symbiont classes that broadly coincided with the convergent evolution of phylogenetically or functionally similar associations in diverse lineages (plants, fungi, bacteria). While a relatively recent loss of lichenization in Lecanoromycetes was previously identified, our work instead suggests lichenization was abandoned far earlier, interrupting what had previously been considered a direct switch between trebouxiophycean and trentepohlialean algal symbionts. Consequently, some of the most diverse clades of LFF are instead derived from nonlichenized ancestors and re-evolved lichenization with Trentepohliales algae, a clade that also facilitated lichenization in unrelated lineages of LFF. Furthermore, while symbiont identity and symbiotic phenotype influence the ecology and physiology of lichens, they are not correlated with rates of lineage birth and death, suggesting more complex dynamics underly lichen diversification. Finally, diversification patterns of LFF differed from those of wood-rotting and ectomycorrhizal taxa, likely reflecting contrasts in their fundamental biological properties. Together, our work provides a timeline for the ecological contributions of lichens, and reshapes our understanding of symbiotic persistence in a classic model of symbiosis.
共生关系在进化上普遍存在，并在构建生态系统中发挥着基本作用，但我们对其宏观进化起源、持续存在和后果的理解并不完整。我们追溯了标志性共生关系——地衣中共生关系和表型多样化的宏观进化历史。通过推断迄今为止最全面的地衣形成真菌（LFF）时间尺度系统发育（超过 3300 种），我们确定了共生体类群之间的转变，这些转变与不同谱系（植物、真菌、细菌）中具有系统发育或功能相似关联的趋同进化大致相符。虽然以前已经确定了 Lecanoromycetes 中地衣化的相对近期丧失，但我们的工作表明地衣化实际上更早被放弃，中断了以前被认为是 trebouxiophycean 和 trentepohlialean 藻类共生体之间的直接转变。因此，一些最具多样性的 LFF 分支来自非地衣化的祖先，并与 Trentepohliales 藻类重新进化为地衣化，而这个藻类分支也促进了 LFF 中不相关谱系的地衣化。此外，虽然共生体身份和共生表型影响地衣的生态和生理学，但它们与谱系出生和死亡的速度没有相关性，这表明地衣多样化的背后存在更复杂的动态。最后，LFF 的多样化模式与木质腐朽和外生菌根分类群的模式不同，这可能反映了它们基本生物学特性的差异。总的来说，我们的工作为地衣的生态贡献提供了一个时间表，并重塑了我们对经典共生关系中共生体持续存在的理解。
