Hosts winnow symbionts with multiple layers of absolute and conditional discrimination mechanisms

In mutualism, hosts select symbionts via partner choice and preferentially
direct more resources to symbionts that provide greater benefits via
sanctions. At the initiation of symbiosis, prior to resource exchange, it
is not known how the presence of multiple symbiont options (i.e., the
symbiont social environment) impacts partner choice outcomes. Furthermore,
little research addresses whether hosts primarily discriminate among
symbionts via sanctions, partner choice or a combination. We inoculated
the legume, Acmispon wrangelianus, with 28 pairs of fluorescently labeled
Mesorhizobium strains that vary continuously in quality as nitrogen-fixing
symbionts. We find that hosts exert robust partner choice, which enhances
their fitness. This partner choice is conditional such that a
strain's success in initiating nodules is impacted by other strains
in the social environment. This social genetic effect is as important as a
strain's own genotype in determining nodulation and has both
transitive (consistent) and intransitive (idiosyncratic) effects on the
probability that a symbiont will form a nodule. Furthermore, both absolute
and conditional partner choice act in concert with sanctions, among and
within nodules. Thus, multiple forms of host discrimination act as a
series of sieves that optimize host benefits and select for costly
symbiont cooperation in mixed symbiont populations.

在互利共生（mutualism）关系中，宿主通过伴侣选择（partner choice）筛选共生体（symbiont），并通过制裁（sanctions）手段优先向提供更高收益的共生体分配更多资源。在共生起始阶段，即资源交换发生之前，学界尚不清楚多重共生体可选对象（即共生体社会环境）的存在会如何影响伴侣选择的结果。此外，鲜有研究探讨宿主主要通过制裁、伴侣选择，还是二者结合的方式来甄别共生体。我们将28组经荧光标记的中慢生根瘤菌（Mesorhizobium）菌株接种至豆科植物（legume）Acmispon wrangelianus（草木犀状百脉根）中，这些菌株作为固氮（nitrogen-fixing）共生体的质量呈连续梯度变化。研究发现，宿主可实施稳健的伴侣选择，该过程能够提升宿主的适合度（fitness）。该伴侣选择具有条件依赖性，即某菌株启动结瘤（nodulation）的成功率会受到社会环境中其他菌株的影响。这种社会遗传效应在决定结瘤概率时，与菌株自身基因型的作用同等重要，且对共生体结瘤概率兼具传递性（transitive，一致性）与非传递性（intransitive，特异性）的影响。此外，绝对伴侣选择与条件伴侣选择均与结瘤内部及结瘤间的制裁机制协同发挥作用。因此，宿主的多种甄别形式如同一系列筛选装置，可优化宿主收益，并在混合共生体种群中筛选出需付出适应成本的共生体合作行为。