Polyploidy, or whole genome duplication, is a common phenomenon in plants, but the establishment and persistence of mixed-ploidy populations remains a paradox. This dissertation explores factors that contribute to the persistence and establishment of mixed-ploidy populations in nature. The first chapter investigates the role of unreduced gametes in neopolyploid establishment and finds that variability in their formation rate can have a significant impact on polyploid establishment and persistence. The second chapter searches for evidence of soil microbes exhibiting ploidy-specificity, a pre-condition for microbe-mediated niche differentiation, a possible stabilizing mechanism contributing to ploidy coexistence. Finally, the third chapter tests for microbe-mediated niche differentiation in a mixed-ploidy population of Larrea tridentata. Using a plant-soil feedback experiment this chapter demonstrates that microbe-mediated niche differentiation can facilitate the coexistence of different ploidy levels. Overall, this dissertation demonstrates there are complex and interrelated factors that contribute to the persistence and establishment of mixed-ploidy populations in nature.
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Why so many polyploids? Accounting for environmental stochasticity in unreduced gamete formation lowers the perceived barriers to polyploid establishment
While polyploids are common in nature, existing models suggest that polyploid establishment should be difficult and rare. We explore this apparent paradox by focussing on the role of unreduced gametes, as their union is the main route for the formation of neopolyploids. Production of such gametes is affected by genetic and environmental factors, resulting in variation in the formation rate of unreduced gametes (u). Once formed, neopolyploids face minority cytotype exclusion (MCE) due to a lack of viable mating opportunities. More than a dozen theoretical models have explored factors that could permit neopolyploids to overcome MCE and become established. Until now, however, none have explored variability in u and its consequences for the rate of polyploid establishment. Here, we determine the distribution that best fits the available empirical data on u. We perform a global sensitivity analysis exploring the consequences of using empirical distributions of u to investigate effects on polyploid establishment. We determined that in many cases, u is best fit by a log-normal distribution. We found environmental stochasticity in u dramatically impacts model predictions when compared to a static u. Our results help reconcile previous modelling results suggesting high barriers to the polyploid establishment with the observation that polyploids are common in nature.
more » « less- NSF-PAR ID:
- 10492620
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Journal of Evolutionary Biology
- ISSN:
- 1420-9101
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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 . -
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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 . -
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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 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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Summary Allopolyploids result from hybridization between different evolutionary lineages coupled with genome doubling. Homoeologous chromosomes (chromosomes with common shared ancestry) may undergo recombination immediately after allopolyploid formation and continue over successive generations. The outcome of this meiotic pairing behavior is dynamic and complex. Homoeologous exchanges (HEs) may lead to the formation of unbalanced gametes, reduced fertility, and selective disadvantage. By contrast, HEs could act as sources of novel evolutionary substrates, shifting the relative dosage of parental gene copies, generating novel phenotypic diversity, and helping the establishment of neo‐allopolyploids. However, HE patterns vary among lineages, across generations, and even within individual genomes and chromosomes. The causes and consequences of this variation are not fully understood, though interest in this evolutionary phenomenon has increased in the last decade. Recent technological advances show promise in uncovering the mechanistic basis of HEs. Here, we describe recent observations of the common patterns among allopolyploid angiosperm lineages, underlying genomic and epigenomic features, and consequences of HEs. We identify critical research gaps and discuss future directions with far‐reaching implications in understanding allopolyploid evolution and applying them to the development of important phenotypic traits of polyploid crops.
