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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.
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Neopolyploidy‐induced changes in giant duckweed ( Spirodela polyrhiza ) alter herbivore preference and performance and plant population performance
Abstract PremisePolyploidy is a widespread mutational process in angiosperms that may alter population performance of not only plants but also their interacting species. Yet, knowledge of whether polyploidy affects plant–herbivore dynamics is scarce. Here, we tested whether aphid herbivores exhibit preference for diploid or neopolyploid plants, whether polyploidy impacts plant and herbivore performance, and whether these interactions depend on the plant genetic background. MethodsUsing independently synthesized neotetraploid strains paired with their diploid progenitors of greater duckweed (Spirodela polyrhiza), we evaluated the effect of neopolyploidy on duckweed's interaction with the water‐lily aphid (Rhopalosiphum nymphaeae). Using paired‐choice experiments, we evaluated feeding preference of the herbivore. We then evaluated the consequences of polyploidy on aphid and plant performance by measuring population growth over multiple generations. ResultsAphids preferred neopolyploids when plants were provided at equal abundances but not at equal surface areas, suggesting the role of plant population surface area in driving this preference. Additionally, neopolyploidy increased aphid population performance, but this result was dependent on the plant's genetic lineage. Lastly, the impact of herbivory on neopolyploid vs. diploid duckweed varied greatly with genetic lineage, where neopolyploids appeared to be variably tolerant compared to diploids, sometimes mirroring the effect on herbivore performance. ConclusionsBy experimentally testing the impacts of polyploidy on trophic species interactions, we showed that polyploidization can impact the preference and performance of herbivores on their plant hosts. These results have significant implications for the establishment and persistence of plants and herbivores in the face of plant polyploidy.
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- Award ID(s):
- 1935410
- PAR ID:
- 10610551
- Publisher / Repository:
- Wiley
- Date Published:
- Journal Name:
- American Journal of Botany
- Volume:
- 111
- Issue:
- 8
- ISSN:
- 0002-9122
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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PremiseAlthough polyploidy has been studied since the early 1900s, fundamental aspects of polyploid ecology and evolution remain unexplored. In particular, surprisingly little is known about how newly formed polyploids (neopolyploids) become demographically established. Models predict that most polyploids should go extinct within the first few generations as a result of reproductive disadvantages associated with being the minority in a primarily diploid population (i.e., the minority cytotype principle), yet polyploidy is extremely common. Therefore, a key goal in the study of polyploidy is to determine the mechanisms that promote polyploid establishment in nature. Because premating isolation is critical in order for neopolylpoids to avoid minority cytotype exclusion and thus facilitate establishment, we examined floral morphology and three common premating barriers to determine their importance in generating reproductive isolation of neopolyploids from diploids. MethodsWe induced neopolyploidy inTrifolium pratenseand compared their floral traits to the diploid progenitors. In addition to shifts in floral morphology, we examined three premating barriers: isolation by self‐fertilization, flowering‐time asynchrony, and pollinator‐mediated isolation. ResultsWe found significant differences in the morphology of diploid and neopolyploid flowers, but these changes did not facilitate premating barriers that would generate reproductive isolation of neopolyploids from diploids. There was no difference in flowering phenology, pollinator visitation, or selfing between the cytotypes. ConclusionsOur results indicate that barriers other than the ones tested in this study—such as geographic isolation, vegetative reproduction, and pistil–stigma incompatibilities—may be more important in facilitating isolation and establishment of neopolyploidT. pratense.more » « less
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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.more » « less
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Summary Recently formed allopolyploid species offer unprecedented insights into the early stages of polyploid evolution. This review examines seven well‐studied neopolyploids (we use ‘neopolyploid’ to refer to very recently formed polyploids, i.e. during the past 300 years), spanning different angiosperm families, exploring commonalities and differences in their evolutionary trajectories. Each neopolyploid provides a unique case study, demonstrating both shared patterns, such as rapid genomic and phenotypic changes, and unique responses to hybridization and genome doubling. While previous studies of these neopolyploids have improved our understanding of polyploidy, significant knowledge gaps remain, highlighting the need for further research into the varied impacts of whole‐genome duplication on gene expression, epigenetic modifications, and ecological interactions. Notably, all of these neopolyploids have spontaneously arisen due to human activity in natural environments, underscoring the profound consequences of polyploidization in a rapidly changing world. Understanding the immediate effects of polyploidy is crucial not only for evolutionary biology but also for applied practices, as polyploidy can lead to novel traits, as well as stress tolerance and increased crop yields. Future research directions include investigating the genetic and epigenetic mechanisms underlying polyploid evolution, as well as exploring the potential of neopolyploids for crop improvement and environmental adaptation.more » « less
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Whole-genome duplication is a common macromutation with extensive impacts on gene expression, cellular function, and whole-organism phenotype. As a result, it has been proposed that polyploids have “general-purpose” genotypes that perform better than their diploid progenitors under stressful conditions. Here, we test this hypothesis in the context of stresses presented by anthropogenic pollutants. Specifically, we tested how multiple neotetraploid genetic lineages of the mostly asexually reproducing greater duckweed (Spirodela polyrhiza) perform across a favorable control environment and 5 urban pollutants (iron, salt, manganese, copper, and aluminum). By quantifying the population growth rate of asexually reproducing duckweed over multiple generations, we found that across most pollutants, but not all, polyploidy decreased the growth rate of actively growing propagules but increased that of dormant ones. Yet, when considering total propagule production, polyploidy increased tolerance to most pollutants, and polyploids maintained population-level fitness across pollutants better than diploids. Furthermore, broad-sense genetic correlations in growth rate among pollutants were all positive in neopolyploids but not so for diploids. Our results provide a rare test and support for the hypothesis that polyploids are more tolerant of stressful conditions and can maintain fitness better than diploids across heterogeneous stresses. These results may help predict that polyploids may be likely to persist in stressful environments, such as those caused by urbanization and other human activities.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1002/ajb2.16301
