Ecological divergence is marked by specific plastic gene expression and distinct rhizosphere among sibling allopolyploid marsh orchids (Dactylorhiza)

Abstract

Phenotypic plasticity, the dynamic adjustment of traits to environmental variations, is crucial for enabling species to exploit broader niches and withstand suboptimal conditions. This adaptability is particularly relevant for newly formed allopolyploids, which possess redundant gene copies and must become established in diverse environments distinct from their parents and other relatives. By evaluating gene expression and root mycobiome among two ecologically divergent sibling allopolyploid marsh orchids (Dactylorhiza majalis and D. traunsteineri) in reciprocal transplants at localities where both species are native, we aimed to understand the drivers of species persistence in the face of interspecific gene flow. Despite consistent abiotic differences characterising the alternative environments at each locality, the majority of gene expression differences between the allopolyploids appears to be plastic. Ecologically relevant processes, such as photosynthesis and transmembrane transport, include some genes that are differentially expressed between the two orchids regardless of the environment, while others change their activity plastically in one species or the other. This suggests that although plasticity helps define the specific ecological range of each sibling allopolyploid, it also mediates gene flow between them, thereby preventing differentiation. Extending our investigations to the root mycobiome, we uncover more diverse fungal communities for either species when grown in the environment with nutrient-poor soils, indicating that both abiotic and biotic factors drive the distribution of sibling marsh orchids. Altogether, our results indicate that plasticity can simultaneously promote diversification and homogenization of lineages, influencing the establishment and persistence of recurrently formed allopolyploid species. Significance statementThis study highlights the role of phenotypic plasticity in the persistence and distribution of sibling allopolyploid marsh orchids (Dactylorhiza majalis s.l.). By examining gene expression and the diversity of root mycobiome across reciprocal transplantations in native environments, we uncover high plasticity that facilitates adaptation and gene flow, thereby promoting both diversification and homogenization. These findings underscore the importance of plasticity in the establishment and long-term survival of allopolyploid species across the landscape.