Jonathan P. Spoelhof’s research while affiliated with Florida Museum of Natural History and other places

Polyploidy is an important evolutionary force, yet epigenetic mechanisms, such as DNA methylation, that regulate genome‐wide expression of duplicated genes remain largely unknown. Here, we use Tragopogon (Asteraceae) as a model system to discover patterns and temporal dynamics of DNA methylation in recently formed polyploids. The naturally occurring allotetraploid Tragopogon miscellus formed in the last 95–100 yr from parental diploids Tragopogon dubius and T. pratensis. We profiled the DNA methylomes of these three species using whole‐genome bisulfite sequencing. Genome‐wide methylation levels in T. miscellus were intermediate between its diploid parents. However, nonadditive CG and CHG methylation occurred in transposable elements (TEs), with variation among TE types. Most differentially methylated regions (DMRs) showed parental legacy, but some novel DMRs were detected in the polyploid. Differentially methylated genes (DMGs) were also identified and characterized. This study provides the first assessment of both overall and locus‐specific patterns of DNA methylation in a recent natural allopolyploid and shows that novel methylation variants can be generated rapidly after polyploid formation. Together, these results demonstrate that mechanisms to regulate duplicate gene expression may arise soon after allopolyploid formation and that these mechanisms vary among genes.

This article is a Commentary on Halabi et al. (2023), 240: 918–927.

Premise: Recently formed allopolyploids Tragopogon mirus and T. miscellus and their diploid parental species, T. dubius, T. porrifolius, and T. pratensis, offer a rare opportunity to study the earliest stages of allopolyploidy. The allopolyploid species have also been resynthesized, allowing comparisons between the youngest possible allopolyploid lineages and their natural, established counterparts. For the first time we compare phenotypic traits on a large scale in Tragopogon diploids, natural allopolyploids, and three generations of synthetic allopolyploids. Methods: Our large common-garden experiment measured traits in growth, development, physiology, and reproductive fitness and analyzed differences between allopolyploids and their parental species and between synthetic and natural allopolyploids. Key results: As in many polyploids, the allopolyploid species had some larger physical traits and a higher capacity for photosynthesis than diploid species. Reproductive fitness traits were variable and inconsistent. Allopolyploids had intermediate phenotypes compared to their diploid parents in several traits, but patterns of variation often varied between allopolyploid complexes. Resynthesized and natural allopolyploid lines generally showed minor to non-existent trait differences. Conclusions: In Tragopogon, allopolyploidy results in some typical phenotypic changes, including gigas effects and increased photosynthetic capacity. Being polyploid did not produce a significant reproductive advantage. Comparisons between natural and synthetic T. mirus and T. miscellus are consistent with very limited, idiosyncratic phenotypic evolution following allopolyploidization. This article is protected by copyright. All rights reserved.

The effects of genetic mutations are influenced by genome structure. Polyploids have more gene or allele copies than diploids, which results in higher tolerance of recessive deleterious mutations. However, this benefit may differ between autopolyploids and allopolyploids and between neopolyploids and older polyploid lineages due to the effects of hybridization and diploidization, respectively. To isolate these effects, we measured the impacts of controlled mutagenesis on reproductive fitness traits in closely related Arabidopsis diploids (A. thaliana), autotetraploids (A. thaliana), and allotetraploids (A. suecica), including both synthetic and natural polyploid lines. Overall, mutagenesis had the largest negative impacts on seed production, while its impacts on germination and survival were negligible. As expected, these effects were much stronger in diploids than in polyploids. The differences between autopolyploids, allopolyploids, and polyploids of different ages were minor—cumulative reproductive fitness did not significantly differ between the treatment and control groups for any polyploid line type. These results suggest that hybridization and polyploid age have not impacted the genomic redundancy of Arabidopsis polyploids enough to significantly alter their aggregate response to mutation, although this effect may differ in older polyploid lineages or in allopolyploids with different levels of divergence between parental subgenomes. This article is protected by copyright. All rights reserved

Polyploidy contributes massively to the taxonomic and genomic diversity of angiosperms, but certain aspects of polyploid evolution are still enigmatic. The establishment of a new polyploid lineage following whole-genome duplication (WGD) is a critical step for all polyploid species, but this process is difficult to identify and observe in nature. Mathematical models offer an opportunity to study this process by varying parameters related to the populations, habitats, and organisms involved in the polyploid establishment process. While several models of polyploid establishment have been published previously, very few incorporate spatial factors, including spatial relationships between organisms, habitat shape, or population density. This study presents a stochastic, spatial model of polyploid establishment that shows how factors such as habitat shape and dispersal type can influence the fixation and persistence of nascent polyploids and modulate the effects of other factors. This model predicts that narrow, constrained habitats such as roadsides and coastlines may enhance polyploid establishment, particularly in combination with frequent clonal reproduction, limited dispersal, and high population density. The similarity between this scenario and the growth of many invasive or colonizing species along disturbed, narrow habitats such as roadsides may offer a partial explanation of the prevalence of polyploidy among invasive species.

Old, climatically buffered, infertile landscapes (OCBILs) have been hypothesized to harbour an elevated number of persistent plant lineages and are predicted to occur across different parts of the globe, interspersed with other types of landscapes. We tested whether the mean age of a plant community is associated with occurrence on OCBILs, as predicted by climatic stability and poor soil environments. Using digitized occurrence data for seed plants occurring in Australia (7033 species), sub-Saharan Africa (3990 species) and South America (44 482 species), regions that comprise commonly investigated OCBILs (Southwestern Australian Floristic Region, Greater Cape Floristic Region and campos rupestres), and phylogenies pruned to match the species occurrences, we tested for associations between environmental data (current climate, soil composition, elevation and climatic stability) and two novel metrics developed here that capture the age of a community (mean tip length and mean node height). Our results indicate that plant community ages are influenced by a combination of multiple environmental predictors that vary globally; we did not find statistically strong associations between the environments of OCBIL areas and community age, in contrast to the prediction for these landscapes. The Cape Floristic Region was the only OCBIL that showed a significant, although not strong, overlap with old communities.

A broad difference in the frequencies of plant and animal polyploidy (whole‐genome duplication, WGD) has been recognized since the early 20th century (e.g., Gates, 1924; Dobzhansky, 1937; Stebbins, 1950), and is generally supported by numerous studies of plant and animal karyotypes, genome sizes, and phylogenies (Otto & Whitton, 2000; Gregory & Mable, 2005).

PREMISE OF THE STUDY Polyploidy has extensively shaped the evolution of plants, but the early stages of polyploidy are still poorly understood. The neoallopolyploid species Tragopogon mirus and T. miscellus are both characterized by widespread karyotypic variation, including frequent aneuploidy and intergenomic translocations. Our study illuminates the origins and early impacts of this variation by addressing two questions: How quickly does karyotypic variation accumulate in Tragopogon allopolyploids following whole‐genome duplication (WGD), and how does the fertility of resynthesized Tragopogon allopolyploids evolve shortly after WGD? METHODS We used genomic in situ hybridization and lactophenol‐cotton blue staining to estimate the karyotypic variation and pollen stainability, respectively, of resynthesized T. mirus and T. miscellus during the first five generations after WGD. KEY RESULTS Widespread karyotypic variation developed quickly in synthetics and resembled that of naturally occurring T. mirus and T. miscellus by generation S4. Pollen stainability in resynthesized allopolyploids was consistently lower than that of natural T. mirus and T. miscellus, as well as their respective diploid progenitor species. Logistic regression showed that mean pollen stainability increased slightly over four generations in resynthesized T. mirus but remained at equivalent levels in T. miscellus. CONCLUSIONS Our results clarify some of the changes that occur in T. mirus and T. miscellus immediately following their origin, most notably the rapid onset of karyotypic variation within these species immediately following WGD.

Polyploidy (whole-genome duplication, WGD) is an integral feature of eukaryotic evolution with two main forms typically recognized, autopolyploidy and allopolyploidy. In plants, a growing body of research contradicts historical assumptions that autopolyploidy is both infrequent and inconsequential in comparison to allopolyploidy. However, the legacy of these assumptions still persists through a lack of research on central facets of autopolyploid evolution. This review highlights recent research that has significantly increased scientific understanding of autopolyploidy. Key advances include: 1) unreduced female gametes contribute disproportionally to polyploidization through the formation of triploids, 2) niche divergence in autopolyploids can occur immediately or gradually after WGD through a diverse set of mechanisms, but broad niche overlap is also common between diploids and autopolyploids, and 3) the degree of genomic and transcriptomic changes following WGD is lower in autopolyploids than allopolyploids, but is highly variable both within and between species in both types of polyploids. We discuss the implications of these and other recent findings, present promising systems for future research, and advocate for expanded research in diverse areas of autopolyploid evolution.