Data_Sheet_2_Nutrient-Poor Breeding Substrates of Ambrosia Beetles Are Enriched With Biologically Important Elements.xlsx

Fungus-farming within galleries in the xylem of trees has evolved independently in at least twelve lineages of weevils (Curculionidae: Scolytinae, Platypodinae) and one lineage of ship-timber beetles (Lymexylidae). Jointly these are termed ambrosia beetles because they actively cultivate nutritional “ambrosia fungi” as their main source of food. The beetles are obligately dependent on their ambrosia fungi as they provide them a broad range of essential nutrients ensuring their survival in an extremely nutrient-poor environment. While xylem is rich in carbon (C) and hydrogen (H), various elements essential for fungal and beetle growth, such as nitrogen (N), phosphorus (P), sulfur (S), potassium (K), calcium (Ca), magnesium (Mg), and manganese (Mn) are extremely low in concentration. Currently it remains untested how both ambrosia beetles and their fungi meet their nutritional requirements in this habitat. Here, we aimed to determine for the first time if galleries of ambrosia beetles are generally enriched with elements that are rare in uncolonized xylem tissue and whether these nutrients are translocated to the galleries from the xylem by the fungal associates. To do so, we examined natural galleries of three ambrosia beetle species from three independently evolved farming lineages, Xyleborinus saxesenii (Scolytinae: Xyleborini), Trypodendron lineatum (Scolytinae: Xyloterini) and Elateroides dermestoides (Lymexylidae), that cultivate unrelated ambrosia fungi in the ascomycete orders Ophiostomatales, Microascales, and Saccharomycetales, respectively. Several elements, in particular Ca, N, P, K, Mg, Mn, and S, were present in high concentrations within the beetles’ galleries but available in only very low concentrations in the surrounding xylem. The concentration of elements was generally highest with X. saxesenii, followed by T. lineatum and E. dermestoides, which positively correlates with the degree of sociality and productivity of brood per gallery. We propose that the ambrosia fungal mutualists are translocating essential elements through their hyphae from the xylem to fruiting structures they form on gallery walls. Moreover, the extremely strong enrichment observed suggests recycling of these elements from the feces of the insects, where bacteria and yeasts might play a role.

在树木木质部中营菌的真菌养殖行为，已在至少十二个豆象科（Curculionidae: Scolytinae, Platypodinae）的种群和一种木质长蠹科（Lymexylidae）的种群中独立演化。这些种群共同被称为食菌甲虫，因为它们积极培育营养丰富的‘食菌真菌’作为其主要食物来源。这些甲虫对其食菌真菌的依赖性是必然的，因为后者为它们提供了广泛的必需营养素，确保它们在极端贫营养环境中的生存。尽管木质部富含碳（C）和氢（H），以及真菌和甲虫生长所必需的各种元素，如氮（N）、磷（P）、硫（S）、钾（K）、钙（Ca）、镁（Mg）和锰（Mn），但这些元素在浓度上却极为低微。目前尚未有实证研究来检验食菌甲虫及其真菌如何在这样的生境中满足其营养需求。在本研究中，我们首次旨在确定食菌甲虫的隧道是否通常富含在未入侵木质部组织中稀少的元素，以及这些营养素是否由真菌共生体从木质部转移到隧道中。为此，我们考察了来自三个独立演化养殖谱系的三种食菌甲虫的自然隧道，分别是 Xyleborinus saxesenii（Scolytinae: Xyleborini）、Trypodendron lineatum（Scolytinae: Xyloterini）和 Elateroides dermestoides（Lymexylidae），它们分别培养与子囊菌纲的 Ophiostomatales、Microascales 和 Saccharomycetales 无关的食菌真菌。一些元素，特别是钙（Ca）、氮（N）、磷（P）、钾（K）、镁（Mg）、锰（Mn）和硫（S），在甲虫隧道中的浓度较高，但在周围木质部中的浓度却极低。元素的浓度通常以 X. saxesenii 为最高，其次是 T. lineatum 和 E. dermestoides，这与隧道中幼虫的社交程度和每隧道的繁殖生产力呈正相关。我们提出，食菌真菌共生体通过其菌丝从木质部将必需元素转移到它们在隧道壁上形成的子实体结构中。此外，观察到的极端富集现象表明，这些元素可能通过昆虫粪便中的循环利用，其中细菌和酵母可能发挥作用。