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Polyploidy is widely acknowledged to have played an important role in the evolution and diversification of vascular plants. However, the influence of genome duplication on population-level dynamics and its cascading effects at the community level remain unclear. In part, this is due to persistent uncertainties over the extent of polyploid phenotypic variation, and the interactions between polyploids and co-occurring species, and highlights the need to integrate polyploid research at the population and community level. Here, we investigate how community-level patterns of phylogenetic relatedness might influence escape from minority cytotype exclusion, a classic population genetics hypothesis about polyploid establishment, and population-level species interactions. Focusing on two plant families in which polyploidy has evolved multiple times, Brassicaceae and Rosaceae, we build upon the hypothesis that the greater allelic and phenotypic diversity of polyploids allow them to successfully inhabit a different geographic range compared to their diploid progenitor and close relatives. Using a phylogenetic framework, we specifically test (1) whether polyploid species are more distantly related to diploids within the same community than co-occurring diploids are to one another, and (2) if polyploid species tend to exhibit greater ecological success than diploids, using species abundance in communities as an indicator of successful establishment. Overall, our results suggest that the effects of genome duplication on community structure are not clear-cut. We find that polyploid species tend to be more distantly related to co-occurring diploids than diploids are to each other. However, we do not find a consistent pattern of polyploid species being more abundant than diploid species, suggesting polyploids are not uniformly more ecologically successful than diploids. While polyploidy appears to have some important influences on species co-occurrence in Brassicaceae and Rosaceae communities, our study highlights the paucity of available geographically explicit data on intraspecific ploidal variation. The increased use of high-throughput methods to identify ploidal variation, such as flow cytometry and whole genome sequencing, will greatly aid our understanding of how such a widespread, radical genomic mutation influences the evolution of species and those around them.
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Neopolyploidy increases stress tolerance and reduces fitness plasticity across multiple urban pollutants: support for the “general-purpose” genotype hypothesis
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.
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- Award ID(s):
- 1935410
- PAR ID:
- 10491727
- Publisher / Repository:
- Oxford
- Date Published:
- Journal Name:
- Evolution Letters
- ISSN:
- 2056-3744
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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.more » « less
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Summary Polyploidy is a key driver of ecological and evolutionary processes in plants, yet little is known about its effects on biotic interactions. This gap in knowledge is especially profound for nutrient acquisition mutualisms, despite the fact that they regulate global nutrient cycles and structure ecosystems. Generalism in mutualistic interactions depends on the range of potential partners (niche breadth), the benefits obtained and ability to maintain benefits across a variety of partners (fitness plasticity). Here, we determine how each of these is influenced by polyploidy in the legume–rhizobium mutualism.We inoculated a broad geographic sample of natural diploid and autotetraploid alfalfa (Medicago sativa) lineages with a diverse panel ofSinorhizobiumbacterial symbionts. To analyze the extent and mechanism of generalism, we measured host growth benefits and functional traits.Autotetraploid plants obtained greater fitness enhancement from mutualistic interactions and were better able to maintain this across diverse rhizobial partners (i.e. low plasticity in fitness) relative to diploids. These benefits were not attributed to increases in niche breadth, but instead reflect increased rewards from investment in the mutualism.Polyploid plants displayed greater generalization in bacterial mutualisms relative to diploids, illustrating another axis of advantage for polyploids over diploids.more » « less
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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.more » « less
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PremisePolyploidy is known to cause physiological changes in plants which, in turn, can affect species interactions. One major physiological change predicted in polyploid plants is a heightened demand for growth‐limiting nutrients. Consequently, we expect polyploidy to cause an increased reliance on the belowground mutualists that supply these growth‐limiting nutrients. An important first step in investigating how polyploidy affects nutritional mutualisms in plants, then, is to characterize differences in the rate at which diploids and polyploids interact with belowground mutualists. MethodsWe usedHeuchera cylindrica(Saxifragaceae) to test how polyploidy influences interactions with arbuscular mycorrhizal fungi (AMF). Here we first confirmed the presence ofAMFinH. cylindrica, and then we used field‐collected specimens to quantify and compare the presence ofAMFstructures while controlling for site‐specific variation. ResultsTetraploids had higher colonization rates as measured by total, hyphal, and nutritional‐exchange structures; however, we found that diploids and tetraploids did not differ in vesicle colonization rates. ConclusionsThe results suggest that polyploidy may alter belowground nutritional mutualisms with plants. Because colonization by nutritional‐exchange structures was higher in polyploids but vesicle colonization was not, polyploids might form stronger associations with theirAMFpartners. Controlled experiments are necessary to test whether this pattern is driven by the direct effect of polyploidy onAMFcolonization.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/evlett/qrad072
