图1 陆地生态系统中植物-微生物互惠共生的演化。a. 在登陆后不久, 陆地植物与内生菌根真菌(AMF)的祖先形成了共生关系(Strullu-Derrien et al, 2014)。图中展示了单个根尖(左, 浅绿色的表皮根细胞和浅棕色的皮层细胞)和AMF菌丝是如何形成细胞内结构的。b. 早期森林出现于木本维管植物占优势的早泥盆纪(Willis & McElwain, 2014)。c. 陆地植物与外生菌根真菌(EMF) (Cairney, 2000; Martin et al, 2016)建立稳定共生关系。EMF是能够分解木质素的腐生真菌的后代, 帮助植物获取有机质中被锁住的养分。d. 受环境条件变化的选择, 早白垩纪出现了有花植物, 是植物适应性创新的一个里程碑(Willis & McElwain, 2014)。e. 植物创新的另一个里程碑事件发生在地下,白垩纪-古近纪界线不久之后(Werner et al, 2015), 植物与固氮菌形成了互惠共生关系。这些细菌(居住在橙色的细胞中)可以打开氮气的三键, 为植物供应可利用的氮。共生关系a、c、e用红色箭头指向地质时间, 地质史关键事件b、d则使用蓝色箭头。该图修改自Lu和Hedin (2019)的图1。a、c、e图作者为孙漪南, b图来自布朗大学的Andrew Lesile, d图来自作者本人。

Fig. 1 Evolution of plant-microbe mutualism in terrestrial ecosystems. a. Land plants formed associations with early ancestors of arbuscular mycorrhizal fungi (AMF) soon after the plant’s colonization of terrestrial ecosystems (Strullu-Derrien et al, 2014). The schematic illustrates how an individual root tip (left, showing epidermal root cells in light green and cortical cells in light brown) and AMF mycelial forms intracellular structure. AMF hyphae is magnitude thinner than even the thinnest plant roots, allowing them superb ability to access soil resources from the porous soil matrix. b. The early forest emerged in the early Devonian after woody vascular plants gained dominance (Willis & McElwain, 2014). c. Land plants formed associations with ectomycorrhizal fungi (EMF) (Cairney, 2000), the descendant of wood-decaying fungi, aiding plants in accessing nutrients that otherwise would be locked into organic matter. d. Selected by the changing environmental condition, flowering plants emerged during the early Cretaceous as a milestone for plants’ adaptive innovation (Willis & McElwain, 2014). e. Another milestone for plant innovation happened belowground, shortly after the Cretaceous-Paleogene boundary Werner et al (2015), with plants forming mutualistic associations with nitrogen-fixing bacteria. These bacteria (housed in these orange cells) can breakdown the triple bond of N2 gas and supply plants with plant available forms of nitrogen. The geological timings of mutualistic relationships a, c, e are indicated by red arrows, while that of geological events b, d by blue arrows. This figure is modified based on Figure 1 in Lu & Hedin (2019). Illustration in a, c, e, from Yinan Sun, b from Andrew Lesile of Brown University, and d from the author.

图2 互惠种群N1和N2的相平面。a. 当雅各比行列式det(J) > 0时, 相互作用导致稳定的非平凡平衡(r1 = r2 = 2, a11 = a22 = -1.5, a12 = a21 = 1)。b. 当雅各比行列式det(J) < 0时, 相互作用导致种群数量无限增长的非稳定动态(r1 = r2 = 2, a11 = a22 = -1.5, a12 = a21 = 2)。种群N1的零增长等值线用绿色, N2的零增长等值线用红色。黑色填充圆表示稳定平衡点, 白色填充圆表示非稳定和半稳定(鞍点)平衡点, 灰色箭头表示种群变化方向。绘图软件Julia 1.4.1。

Fig. 2 Phase planes of mutualistic interactions between population N1 and N2. a. The mutualistic interaction leads to stable nontrivial equilibrium when det(J) > 0 (r1 = r2 = 2, a11 = a22 = -1.5, a12 = a21 = 1). b. The mutualistic interaction leads to non-stable dynamics (infinite populations size) when det(J) < 0 (r1 = r2 = 2, a11 = a22 = -1.5, a12 = a21 = 2). The nullcline of population N1 is labeled in green and N2 in red. Black-filled circle denotes stable equilibrium while white-filled circles denote non-stable and half-stable (saddle points) equilibria. Plots are made in Julia 1.4.1.

图3 迭代囚徒困境(IDP) (a)与生物市场理论(BMT) (b)的图形说明以及BMT的核心概念(c)。a. 两个玩家随着时间的推移以对称的方式重复互动, 每个玩家都能够记住最近一次的互动。玩家被标记为相同的填充点, 强调了这种方法固有的对称性(例如, 蝙蝠之间的种内合作)。b. 两组玩家通过类似于二分网络的形式进行交互作用, 其中一组中的每个玩家都可以与来自另一组的多个玩家进行交互(为了简化视觉, 这里只显示了部分交互)。这两个组在这里用不同的符号表示(正方形和三角形), 以强调这种方法内在的不对称性, 这使得它在处理特定种间的互惠互动(例如, 植物与微生物, 蜜蜂与花)时很有优势。BMT模型的最小设置用浅红色标记, 一共三个玩家, 其中一个玩家与另外两个玩家交互。c. 生物市场理论里面的最重要基本概念可以从生态时间尺度分成两类(实线时间轴): 合作伙伴选择和伴侣忠诚反馈。这两类概念所对应的生物学过程在进化时间尺度上是相连的(虚线)。

Fig. 3 Graphical illustration of Iterated Prisoner’s Dilemma (IDP) (a) vs. Biological Market Theory (BMT) (b), and core concepts used in BMT (c). a. Two players interact in a symmetric manner repeatedly over time, with each player being able to remember interactions from the immediate last time step. The players are denoted with the same filled dots, emphasizing the symmetry inherent to this approach (for example, intraspecific cooperation between individual bats). b. Two classes of players interact through a bipartite-graph alike interaction, where each player in one class can interact with multiple players from the other class (for visual simplicity, only part of the interactions are shown here). The two classes are denoted with different symbols here to emphasize the inherent asymmetry of this approach, which makes it unique in dealing with inter-specific mutualistic interaction (for example, plants vs. microbes, bees vs. flowers). The minimal setup of a BMT model is labeled in light red, where 1 player interacts with 2 other. c. The most fundamental concepts in BMT can be divided into two broad classes based on timescale (solid time arrow): partner choice vs. partner fidelity feedback. The biological processes represented by these two classes of concepts are linked over evolutionary time (dashed line).

图4 双稳态植被格局及植物-微生物互惠共生的作用。a、b为植被斑块的景观图, 其中互惠共生类型A和B (在这种情况下, 丛枝菌根与外生菌根植物)的丰富度表示为色块的灰度。a所呈现的景观中, 双稳态植被状态是存在的, 一块植被要么是A主导要么是B主导, 而b则是两种互惠共生类型的随机混合。c、d互惠共生关系的分布可以用从beta分布中提取的5,000个随机数(代表5,000个景观斑块)的频率分布来说明:$f(y:\mu, phi)=cy^{\mu\varphi-1} (1-y)^{(1-\mu)\varphi-1}$ (y表示A的百分比, μ作为集中趋势, ?为离散系数)。c图所示的双峰大体可以描绘a图色块的频率分布, 而d图的单峰分布可以描绘b图色块的频率分布。e图表示A和B的初始成分(小点)随着时间的推移而分化成两种不同的稳定状态(大点, 紫色表示EMF, 绿色表示AMF)。图c、d、e摘自Lu和Hedin (2019)。

Fig. 4 Bistable vegetation patterns and the role of plant-microbe mutualism. a, b. An illustration of a landscape with patches of vegetation, where the abundance of mutualistic interaction A and B (in this case, Arbuscular mycorrhizal vs. ectomycorrhizal symbioses) is denoted by the darkness of the gray hue. a presents a landscape where bistable vegetation states is found where you either find a patch of vegetation extremely high or extremely low in one type of mutualism, whereas b has a mixture of both mutualistic type in each patch. c, d. The distribution of mutualist abundance can be illustrated using the frequency distribution of 5,000 random numbers (representing 5,000 landscape patches) drawn from a beta distribution: $f(y:\mu, phi)=cy^{\mu\varphi-1} (1-y)^{(1-\mu)\varphi-1}$ (y indicates percentage of A, μ as the central tendency, and ? as the dispersion coefficient). e. Patches that have different founding composition (small dots) of A and B will over time diverge into two alternative stable states (larger dot, EMF indicated in purple and AMF indicated in green). Panels c, d, e are reproduced from figures published in Lu & Hedin (2019).