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 plant
- Award ID(s):
- 1550813
- NSF-PAR ID:
- 10082221
- Date Published:
- Journal Name:
- Frontiers in ecology and evolution
- Volume:
- 6
- ISSN:
- 2296-701X
- Page Range / eLocation ID:
- 52
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Spirodela polyrhiza using 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. -
Premise of the Study Polyploidy, or whole genome duplication (
WGD ), is common in plants despite theory suggesting that polyploid establishment is challenging and polyploids should be evolutionarily transitory. There is renewed interest in understanding the mechanisms that could facilitate polyploid establishment and explain their pervasiveness in nature. In particular, premating isolation from their diploid progenitors is suggested to be a crucial factor. To evaluate how changes in assortative mating occur, we need to understand the phenotypic effects ofWGD on reproductive traits.Methods We used literature surveys and a meta‐analysis to assess how
WGD affects floral morphology, flowering phenology, and reproductive output in plants. We focused specifically on comparisons of newly generated polyploids (neopolyploids) and their parents to mitigate potential confounding effects of adaptation and drift that may be present in ancient polyploids.Key Results The results indicated that across a broad representation of angiosperms, floral morphology traits increased in size, reproductive output decreased, and flowering phenology was unaffected by
WGD . Additionally, we found that increased trait variation afterWGD was uncommon for the phenotypic traits examined.Conclusions Our results suggest that the phenotypic effects on traits important to premating isolation of neopolyploids are small, in general. Changes in flowering phenology, reproductive output, and phenotypic variation resulting from
WGD may be less critical in facilitating premating isolation and neopolyploid establishment. However, floral traits for which size is an important component of function (e.g., pollen transfer) could be strongly influenced byWGD . -
Premise Although 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.
Methods We induced neopolyploidy in
Trifolium pratense and 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.Results We 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.
Conclusions Our 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 neopolyploid
T. pratense . -
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 plant
Spirodela 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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null (Ed.)Floral organ size, especially the size of the corolla, plays an important role in plant reproduction by facilitating pollination efficiency. Previous studies have outlined a hypothesized organ size pathway. However, the expression and function of many of the genes in the pathway have only been investigated in model diploid species; therefore, it is unknown how these genes interact in polyploid species. Although correlations between ploidy and cell size have been shown in many systems, it is unclear whether there is a difference in cell size between naturally occurring and synthetic polyploids. To address these questions comparing floral organ size and cell size across ploidy, we use natural and synthetic polyploids of Nicotiana tabacum (Solanaceae) as well as their known diploid progenitors. We employ a comparative transcriptomics approach to perform analyses of differential gene expression, focusing on candidate genes that may be involved in floral organ size, both across developmental stages and across accessions. We see differential expression of several known floral organ candidate genes including ARF2, BIG BROTHER, and GASA/GAST1. Results from linear models show that ploidy, cell width, and cell number positively influence corolla tube circumference; however, the effect of cell width varies by ploidy, and diploids have a significantly steeper slope than both natural and synthetic polyploids. These results demonstrate that polyploids have wider cells and that polyploidy significantly increases corolla tube circumference.more » « less