O'Donnell Ryan P, Wong Darren C J, Phillips Ryan D, Peakall Rod, Linde Celeste C
Division of Ecology and Evolution, Research School of Biology, 46 Sullivans Creek Road, The Australian National University, Canberra, Australian Capital Territory, 2600, Australia.
School of Agriculture, Food, and Wine, Waite Research Precinct, University of Adelaide, Adelaide, South Australia, 5064, Australia.
Syst Biol. 2025 Jun 12;74(3):434-452. doi: 10.1093/sysbio/syae070.
Orchid mycorrhizal fungi (OMF) associations in the Orchidaceae are thought to have been a major driver of diversification in the family. In the terrestrial orchid tribe Diurideae, it has long been hypothesized that OMF symbiont associations may reflect evolutionary relationships among orchid hosts. Given that recent phylogenomic efforts have been unable to fully resolve relationships among subtribes in the Diurideae, we sought to ascertain whether orchid OMF preferences may lend support to certain phylogenetic hypotheses. First, we used phylogenomic methods and Bayesian divergence time estimation to produce a genus-level tree for the Diurideae. Next, we synthesized decades of published fungal sequences and morphological/germination data to identify dominant fungal partners at the genus scale and perform ancestral state reconstruction to estimate the evolutionary trajectory of fungal symbiont shifts. Across the tribe, we found phylogenomic discordance stemming from incomplete lineage sorting. However, our results also revealed unprecedented phylogenetic niche conservatism of fungal symbionts within the tribe: entire genera, subtribes, and even groups of related subtribes associate with only a single fungal family, suggesting that fungal symbiont preferences in the Diurideae do indeed reflect phylogenetic relationships among orchid hosts. Moreover, we show that these relationships have evolved directionally from generalist associations with multiple fungal families towards more specific partnerships with only one fungal family. Orchid symbiont preferences here provide new insights into the placement of several groups with longstanding phylogenetic uncertainty. In spite of complex evolutionary histories, host-symbiont relationships can be used to help detangle alternative phylogenetic hypotheses.
兰科植物中的兰花菌根真菌（OMF）共生关系被认为是该科植物多样化的主要驱动力。在陆生兰花部落双蕊兰族中，长期以来一直有人假设OMF共生体关联可能反映兰花宿主之间的进化关系。鉴于最近的系统发育基因组学研究未能完全解决双蕊兰族亚族之间的关系，我们试图确定兰花对OMF的偏好是否可能支持某些系统发育假说。首先，我们使用系统发育基因组学方法和贝叶斯分歧时间估计来构建双蕊兰族的属级系统发育树。接下来，我们综合了数十年来已发表的真菌序列以及形态学/萌发数据，以确定属水平上的主要真菌伙伴，并进行祖先状态重建，以估计真菌共生体转移的进化轨迹。在整个部落中，我们发现由于不完全谱系分选导致的系统发育不一致。然而，我们的结果还揭示了该部落内真菌共生体前所未有的系统发育生态位保守性：整个属、亚族，甚至相关亚族组仅与一个真菌科相关联，这表明双蕊兰族中真菌共生体的偏好确实反映了兰花宿主之间的系统发育关系。此外，我们表明这些关系已经从与多个真菌科的泛化关联朝着仅与一个真菌科的更特定伙伴关系定向进化。这里兰花共生体的偏好为几个长期存在系统发育不确定性的类群的位置提供了新的见解。尽管进化历史复杂，但宿主-共生体关系可用于帮助理清替代的系统发育假说。
