Decreased coevolutionary potential and increased symbiont fecundity during the biological invasion of a legume-rhizobium mutualism

Although most invasive species engage in mutualism, we know little about how mutualism evolves as partners colonize novel environments. Selection on cooperation and standing genetic variation for mutualism traits may differ between a mutualism's invaded and native ranges, which could alter cooperation and coevolutionary dynamics. To test for such differences, we compare mutualism traits between invaded- and native-range host-symbiont genotype combinations of the weedy legume, Medicago polymorpha, and its nitrogen-fixing rhizobium symbiont, Ensifer medicae, which have co-invaded North America. We find that mutualism benefits for plants are indistinguishable between invaded- and native-range symbioses. However, rhizobia gain greater fitness from invaded-range mutualisms than from native-range mutualisms, and this enhancement of symbiont fecundity could increase the mutualism’s spread by increasing symbiont availability during plant colonization. Furthermore, mutualism traits in invaded-range symbioses show lower genetic variance and a simpler partitioning of genetic variance between host and symbiont sources, compared to native-range symbioses. This suggests that biological invasion has reduced mutualists’ potential to respond to coevolutionary selection. Additionally, rhizobia bearing a locus (hrrP) that can enhance symbiotic fitness have more exploitative phenotypes in invaded-range than in native-range symbioses. These findings highlight the impacts of biological invasion on the evolution of mutualistic interactions.

Methods
We generated a collection of Ensifer medicae (rhizobia) strains from field soils and used PCR to screen each strain for the presence of hrrP, a gene that can change how cooperative rhizobia are with their legume hosts. We provide the results of the PCR screen for each strain in our collection. A subset of rhizobia from this collection was inoculated onto Medicago polymorpha plants in a greenhouse experiment, and we measured plant growth benefits from inoculation (leaf count, shoot mass) and symbiosis traits (number of root nodules, nodule size, and number of colony-forming units of E. medicae within the nodules). We provide raw plant-level and nodule-level data from this experiment.

尽管多数入侵物种均形成互利共生关系，但我们对共生伙伴入驻新环境时共生体系的演化机制仍缺乏深入认知。合作相关的选择压力与共生性状的现存遗传变异，在共生体系的入侵分布范围与原生分布范围之间可能存在差异，这或许会改变合作模式与共进化动态。为检验这类差异，我们针对共同入侵北美地区的杂草状豆科植物蒺藜苜蓿（Medicago polymorpha）与其固氮根瘤菌共生体苜蓿中华根瘤菌（Ensifer medicae）的入侵范围与原生范围宿主-共生体基因型组合的共生性状开展了对比分析。

研究发现，入侵范围与原生范围的共生体系对植物的共生收益并无显著差异。但根瘤菌从入侵范围的共生体系中获得的适合度更高，这种共生体繁殖能力的提升可通过提高植物定殖阶段的共生体可获得性，促进共生体系的扩散。此外，与原生范围的共生体系相比，入侵范围共生体系的共生性状遗传方差更低，宿主与共生体间的遗传方差分区模式也更为简洁。这表明生物入侵降低了共生者响应共进化选择的潜力。进一步研究发现，携带可提升共生适合度的hrrP基因座（hrrP）的根瘤菌，在入侵范围的共生体系中表现出比原生范围更强的剥削性表型。上述研究结果揭示了生物入侵对互利共生相互作用演化的影响。

**方法**
我们从田间土壤中分离得到一系列苜蓿中华根瘤菌（Ensifer medicae，根瘤菌）菌株，并通过聚合酶链式反应（PCR）筛选各菌株是否携带hrrP基因——该基因可调控根瘤菌与豆科宿主的合作程度。我们提供了本研究菌株集合的全部PCR筛选结果。我们选取该菌株集合中的部分根瘤菌菌株，在温室实验中接种蒺藜苜蓿（Medicago polymorpha）植株，测定接种带来的植物生长收益（叶片数、地上部生物量）以及共生性状（根瘤数量、根瘤大小以及根瘤内苜蓿中华根瘤菌的菌落形成单位数）。本研究同时提供该实验的植株水平与根瘤水平原始数据。