Data from: Know your farmer: ancient origins and multiple independent domestications of ambrosia beetle fungal cultivars

Bark and ambrosia beetles are highly specialized weevils (Curculionidae) that have established diverse symbioses with fungi, most often from the order Ophiostomatales (Ascomycota, Sordariomycetes). The two types of beetles are distinguished by their feeding habits and intimacy of interactions with their symbiotic fungi. The tree tissue diet of bark beetles is facilitated by fungi, while ambrosia beetles feed solely on fungi that they farm. The farming life history strategy requires domestication of a fungus, which the beetles consume as their sole food source. Ambrosia beetles in the subfamily Platypodinae originated in the mid-Cretaceous (119-88Mya) and are the oldest known group of farming insects. However, attempts to resolve phylogenetic relationships and the timing of domestication events for fungal cultivars have been largely inconclusive. We sequenced the genomes of 12 ambrosia beetle fungal cultivars and bark beetle associates, including the devastating laurel wilt pathogen, Raffaelea lauricola, to estimate a robust phylogeny of the Ophiostomatales. We find evidence for contemporaneous diversification of the beetles and their associated fungi, followed by three independent domestication events of the ambrosia fungi genus Raffaelea. We estimate the first domestication of an Ophiostomatales fungus occurred ~86Mya, 25 million years earlier than prior estimates and in close agreement with the estimated age of farming in the Platypodinae (96Mya). Comparisons of the timing of fungal domestication events with the timing of beetle radiations support the hypothesis that the first large beetle radiations may have spread domesticated ‘ambrosia’ fungi to other fungi-associated beetle groups, perhaps facilitating the evolution of new farming lineages.

树皮小蠹与食菌小蠹均为高度特化的象鼻虫（weevils），隶属于象甲科（Curculionidae），二者与真菌建立了多样的共生关系，共生伙伴多隶属于长喙壳菌目（Ophiostomatales，子囊菌门Ascomycota，粪壳菌纲Sordariomycetes）。两类甲虫可通过取食习性以及与共生真菌的互作紧密程度加以区分：树皮小蠹依赖真菌协助获取树木组织作为食物，而食菌小蠹则仅以自身培育的真菌为食。这种培育型生活史策略需要甲虫驯化一种真菌，并将其作为唯一的食物来源。隶属于长小蠹亚科（Platypodinae）的食菌小蠹起源于白垩纪中期（119-88Mya，即1.19亿至0.88亿年前），是目前已知最古老的培育型昆虫类群。然而，此前针对真菌栽培菌种的系统发育关系及驯化事件时间节点的解析，大多未能得到明确结论。本研究对12种食菌小蠹的共生真菌以及树皮小蠹的伴生真菌进行了基因组测序，其中包括极具破坏性的樟叶枯萎病原菌——樟枯萎红喙孢（Raffaelea lauricola），以此构建长喙壳菌目可靠的系统发育树。研究结果表明，甲虫与其共生真菌存在协同分化现象，随后食菌真菌类群中的红喙孢属（Raffaelea）经历了三次独立的驯化事件。我们估算，长喙壳菌目真菌的首次驯化发生在约8600万年前，比此前的估算结果早2500万年，且与长小蠹亚科培育行为的估算起源时间（96Mya，即0.96亿年前）高度吻合。通过比对真菌驯化事件与甲虫辐射演化的时间节点，研究结果支持以下假说：首次大规模甲虫辐射演化可能将已驯化的‘食菌’真菌传播至其他与真菌相关的甲虫类群，进而推动了全新培育谱系的演化。