Aim Mutualisms are often disrupted for plants introduced to new ranges, yet many of these plants have managed to obtain effective mutualistic associations in their new ranges. There are two potential pathways for non‐native plants to reassemble mutualisms: cointroduction (i.e. familiar associations with cointroduced mutualists) or ecological fitting (i.e. forming or adapting novel associations with resident native mutualists). We assessed the importance of each pathway for mutualist reassembly in four Australian Acacia species (A. baileyana, A. dealbata, A. decurrens and A. melanoxylon) and their associated nitrogen‐fixing rhizobial symbionts in two non‐native locations. Location Native ranges of acacias in south‐eastern Australia and two non‐native ranges in New Zealand and South Africa. Methods Rhizobia associated with each acacia species in each country were isolated and identified based on DNA sequencing of the housekeeping recA gene and the symbiotic nodA gene. Separate phylogenies were reconstructed for each gene region to infer biogeographic histories of acacia‐associated rhizobia. Selected rhizobial strains for each acacia species by country combination were used as inocula in a glasshouse experiment and early growth kinetics and nitrogen fixation efficiency of acacia seedlings were compared between inoculum treatments to determine symbiotic effectiveness. Results All isolated rhizobial strains belonged to the genus Bradyrhizobium. Phylogenetic analyses revealed almost no country‐ or species‐specific clusters of these strains for either gene region and indicated that most acacia‐associated bradyrhizobia in New Zealand and South Africa were cointroduced from Australia. These results were supported by little variation in the growth performances of acacia seedlings, irrespective of inoculum treatment. Main conclusions This study revealed that cointroduction of Australian acacias and their rhizobia may be more prevalent than previously thought. Additionally, a single rhizobium cointroduction event may be sufficient to facilitate the establishment of effective mutualisms in numerous Acacia species, potentially leading to an invasion meltdown.

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Mutualisms can be disrupted when non-native plants are introduced into novel environments, potentially impacting their establishment success. Introduced species can reassemble mutualisms by forming novel associations with resident biota or by maintaining familiar associations when they are co-introduced with their mutualists. Invasive Australian Acacia species in South Africa have formed nitrogen-fixing rhizobium mutualisms using both pathways. Here we examined the contributions of novel vs familiar rhizobial associations to the performance of Acacia saligna across different soils within South Africa’s Core Cape Subregion (CCR), and the concomitant impacts of exotic rhizobia on the endemic legume, Psoralea pinnata. We grew each legume with and without Australian Bradyrhizobium strains across various CCR soil types in a glasshouse. We identified root nodule rhizobium communities associating with seedlings grown in each treatment combination using next-generation sequencing (NGS) techniques. Our results show that different CCR soils affected growth performances of seedlings for both species while the addition of Australian bradyrhizobia affected growth performances of A. saligna, but not P. pinnata. NGS data revealed that each legume associated mostly with their familiar rhizobial partners, regardless of soil conditions or inoculum treatment. Acacia saligna predominantly associated with Australian bradyrhizobia, even when grown in soils without inoculum, while P. pinnata largely associated with native South African Mesorhizobium strains. Our study suggests that exotic Australian bradyrhizobia are already present and widespread in pristine CCR soils, and that mutualist limitation is not an impediment to further acacia invasion in the region. The ability of P. pinnata to sanction Australian Bradyrhizobium strains suggests that this species may be a good candidate for restoration efforts following the removal of acacias in CCR habitats.