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Abstract Whole‐genome duplication has long been appreciated for its role in driving phenotypic novelty in plants, often altering the way organisms interface with the abiotic environment. Only recently, however, have we begun to investigate how polyploidy influences interactions of plants with other species, despite the biotic niche being predicted as one of the main determinants of polyploid establishment. Nevertheless, we lack information about how polyploidy affects the diversity and composition of the microbial taxa that colonize plants, and whether this is genotype‐dependent and repeatable across natural environments. This information is a first step towards understanding whether the microbiome contributes to polyploid establishment. We, thus, tested the immediate effect of polyploidy on the diversity and composition of the bacterial microbiome of the aquatic plantSpirodela polyrhizausing four pairs of diploids and synthetic autotetraploids. Under controlled conditions, axenic plants were inoculated with pond waters collected from 10 field sites across a broad environmental gradient. Autotetraploids hosted 4%–11% greater bacterial taxonomic and phylogenetic diversity than their diploid progenitors. Polyploidy, along with its interactions with the inoculum source and genetic lineage, collectively explained 7% of the total variation in microbiome composition. Furthermore, polyploidy broadened the core microbiome, with autotetraploids having 15 unique bacterial taxa in addition to the 55 they shared with diploids. Our results show that whole‐genome duplication directly leads to novelty in the plant microbiome and importantly that the effect is dependent on the genetic ancestry of the polyploid and generalizable over many environmental contexts. 

Summary Ecological theory predicts that early generation polyploids (‘neopolyploids’) should quickly go extinct owing to the disadvantages of rarity and competition with their diploid progenitors. However, polyploids persist in natural habitats globally. This paradox has been addressed theoretically by recognizing that reproductive assurance of neopolyploids and niche differentiation can promote establishment. Despite this, the direct effects of polyploidy at the population level remain largely untested despite establishment being an intrinsically population‐level process.We conducted population‐level experiments where life‐history investment in current and future growth was tracked in four lineage pairs of diploids and synthetic autotetraploids of the aquatic plantSpirodela polyrhiza. Population growth was evaluated with and without competition between diploids and neopolyploids across a range of nutrient treatments.Although neopolyploid populations produce more biomass, they reach lower population sizes and have reduced carrying capacities when growing alone or in competition across all nutrient treatments. Thus, contrary to individual‐level studies, our population‐level data suggest that neopolyploids are competitively inferior to diploids. Conversely, neopolyploid populations have greater investment in dormant propagule production than diploids.Our results show that neopolyploid populations should not persist based on current growth dynamics, but high potential future growth may allow polyploids to establish in subsequent seasons.