Can plant-fungal symbioses underpin plant diversity?

自从达尔文的开创性工作以来，我们对物种起源（物种形成）的理解发生了很大的变化。然而，有一个方面被忽略了，那就是微生物在推动物种形成中所起的作用。在这里，我们提出了一种新的物种起源机制，即植物-菌根结合的共同进化分歧增加了局部适应并导致物种形成的完成，使用面对基因流的物种形成的最引人注目的例子之一作为我们的模型系统：Lord Howe岛的Howea棕榈树。虽然众所周知，物种可以因山脊或海洋等地理障碍而分化，但种群也可以在没有地理隔离的情况下面对基因流动而分裂，例如通过对栖息地或资源的专业化。在这种情况下，植物与微生物的共生关系可能特别强大，可以同时促进局部适应和生殖隔离，从而导致物种形成。我们将重点研究两种棕榈树的姊妹种（Howea），它们是塔斯曼海中一个偏远岛屿Lord Howe岛的特有物种，以及它们与丛枝菌根真菌的相互作用。然而，棕榈树是岛上的主要植被。Howea的物种形成情景涉及到对不同土壤、火山岩和钙质沉积物的适应，以及相关的适应性权衡。我们假设土壤和土壤微生物影响了祖先棕榈种群的局部适应，从而导致开花时间的差异，并最终促进物种形成。不同水平的菌根定植和基因表达共同调控的豪亚和菌根关联可能导致不同形式的豪亚种群占据不同的土壤的出现。我们将使用宏基因组学和RNA-seq结合在Lord Howe岛的长期实地实验来验证这些关键假设。提出的工作有可能带来对物种形成机制和共同进化如何促进物种分化的激烈反思。这项提议的工作将揭示一些在进化中最被忽视的假设，例如微生物如何驱动植物物种形成，以及微生物组和植物多样性之间的联系。鉴于植物-菌根共生的广泛性，它们在作物生产中的重要性，以及土壤和植物多样性在生态系统功能中的突出地位，我们的研究也将在应用生态学和农业领域产生深远的影响，而不仅仅是进化生物学。

Our understanding of how species originate (speciation) has changed considerably since Darwin's seminal work. One aspect, however, that has been ignored is the role that microbes can play in driving speciation. Here, we propose a new mechanism for the origin of species, whereby coevolutionary divergence in plant-mycorrhizal associations increases local adaptation and leads to the completion of speciation, using one of the most compelling examples of speciation in the face of gene flow as our model system: The Howea palms of Lord Howe Island. While it is well known that species can diverge due to geographic barriers such as mountain ridges or oceans, populations can also split in the face of gene flow without geographic isolation, for example through specialisation to habitats or resources. In this context, symbiotic associations that plants have with microbes may be particularly powerful in simultaneously facilitating local adaptation and reproductive isolation leading to speciation. We will focus on two sister species of palms (Howea), endemic to Lord Howe Island, a remote island in the Tasman sea, and their interactions with arbuscular mycorrhizal fungi. Howea palms represent the dominant vegetation on the island. The speciation scenario for Howea involves adaptation to different soils, volcanic rocks and calcareous deposits, and associated fitness trade-offs. We hypothesise that soil and soil microbes have affected local adaptation of the ancestral palm population, which in turn led to differences in flowering time, and ultimately promoted speciation. Differing levels of mycorrhizal colonisation and gene expression co-regulated in Howea and mycorrhizal associations may have led to the emergence of distinct forms of Howea populations occupying different soils. We will test these key hypotheses using metagenomics and RNA-seq combined with long-term field experiments on Lord Howe Island. The proposed work has the potential to bring drastic rethinking about the mechanisms of speciation and how coevolution contributes to species divergence. The proposed work will unravel some of the most neglected hypotheses in evolution, such as how microbes can drive plant speciation, and hence the link between microbiome and plant diversity. Given the widespread nature of plant-mycorrhizal symbioses, their importance in crop production, and the prominence of soil and plant diversity in ecosystem functioning, our research will also have far-reaching impact in applied ecology and agriculture, beyond evolutionary biology.