Interspecific selection and local adaptation combine to influence Pinus radiata root microbiome associations

Background Microbiomes have co-evolved with endemic trees over millions of years. However, when these trees are planted beyond their native ranges, it remains unclear whether their below-ground microbial relationships persist or change to reflect to local soil communities. Pinus radiata , with its limited endemic range, has been widely introduced to diverse environments globally, providing a unique opportunity to test how microbiomes are shaped by evolutionary processes versus local environmental adaptation. To investigate this, root and soil samples were collected from endemic regions (Mexico and USA) and introduced regions (Australia and New Zealand), alongside environmental and soil physicochemical data. Results Bacterial and fungal communities showed limited taxonomic overlap between endemic and introduced ranges. Both bacterial and fungal root microbiomes were shaped by local drivers, interspecific selection (range) and local adaptation (region), rather than site specific drivers. For bacterial communities, variation explained by local adaptation (15.8%) was greater than that explained by interspecific selection (11.2%). In contrast, these two processes contributed almost equally to fungal communities (19.8% and 19.3%), indicating that evolutionary processes have had a relatively stronger influence on fungal root microbiome assembly than on bacterial communities. Site-specific factors, particularly the composition of the bulk soil microbiome, strongly influenced bacterial communities in roots, accounting for 21.5% of observed variance. This suggests secondary effects of plant species on soil conditions, especially via changes in soil pH, were important drivers of community structure. Despite limited taxonomic overlap, a small set of core taxa were conserved between endemic and introduced ranges, contributing disproportionately to overall community structure, highlight the ecological significance of conserved taxa. Microbial network structures were broadly conserved across ranges but differed in topology. Bacterial networks in introduced regions were more connected and efficient, while fungal networks remained strongly host-filtered yet displayed greater modularity and dispersion, thus suggesting fungal communities may have adopted more flexible or exploratory structures in response to novel conditions. Conclusions This work provides evidence that tree root microbial assembly processes vary across geographic space, shaped by both site-level environmental variation and evolutionary history. We demonstrate a dynamic interplay between plant, soil environment, and the microbiome. These findings provide insights into microbiome adaptability and offer a foundation for managing forest ecosystems for resilience under changing conditions. The success of P. radiata in its introduced range appears to be supported by its ability to engage with the microbiome community composition that draw on both evolutionary legacy and local adaptation, enabling successful microbial associations in diverse environments.