Autopolyploid establishment depends on life-history strategy and the mating outcomes of clonal architecture.

Polyploidy is a significant component in the evolution of many taxa, particularly plant groups. However, new polyploids face substantial fitness disadvantages due to a lack of same-cytotype mates, and the factors promoting or preventing polyploid establishment in natural populations are often unclear. We develop spatially explicit agent-based simulation models to test the hypothesis that a perennial life history and clonal propagation facilitate the early stages of polyploid establishment and persistence. Our models show that polyploids are more likely to establish when they have longer life spans than diploids, especially when self-fertilization rates are high. Polyploids that combine sexual and clonal reproduction can establish across a wide range of life histories, but their success is moderated by clonal strategy. By tracking individuals and mating events, we reveal that clonal architecture has a substantial impact on the spatial structure of the mixed diploid-polyploid population during polyploid establishment: altering patterns of mating within or between cytotypes via geitonogamous self-fertilization, the mechanisms through which polyploid establishment proceeds, and the final composition of the polyploid population. Overall, our findings provide novel insight into the role of clonal structure in modulating the complex relationship between polyploidy, perenniality, and clonality and offer testable predictions for future empirical work.

Polyploidy in urban environments.

Polyploidy is a major driver of evolutionary change in plants, but many aspects of polyploidy in natural systems remain enigmatic. We argue that urban landscapes present an unprecedented opportunity to observe polyploidy in action. Integrating polyploid biology and urban evolutionary ecology, we discuss multiple factors expected to promote polyploid formation, establishment, and persistence in urban systems. We develop a predictive framework for the contemporary ecology and evolution of polyploid plants in cities, and through this novel perspective propose that studying polyploidy in an urban context could lead to breakthroughs in understanding fundamental processes in polyploid evolution. We conclude by highlighting the potential consequences of polyploidy in urban environments, and outline a roadmap for research into this currently unexplored field.

Evolutionary associations between polyploidy, clonal reproduction, and perenniality in the angiosperms.

Clonal reproduction is thought to facilitate polyploid establishment in the angiosperms, but the evolutionary relationship between polyploidy and clonality has not been thoroughly tested. A perennial life history may confer many of the same advantages, and the relative importance of clonality versus perenniality is unknown. We used phylogenetic comparative analyses of 1751 species to examine associations between polyploidy, clonality, and life history. We test hypotheses of co-evolution by determining the sequence of trait development. Polyploidy is associated with both clonality and perenniality across species, and analyses show that clonality can be an important predictor of polyploidy beyond perenniality. Tests of directionality on our full dataset suggest that polyploidy is more likely to promote clonality or perenniality than vice versa, although there are significant differences in patterns of co-evolution among major angiosperm groups. Our results suggest that polyploidy and clonal reproduction are evolutionarily associated across the angiosperms, even when perenniality is considered, but we find little evidence at the whole-angiosperm level for the hypothesis that clonality promotes polyploidy. However, variation among different clades indicates that polyploidy and clonality are interacting in diverse ways, likely to be due to the variable roles of clonality in their evolutionary histories.

Whole-genome duplication decreases clonal stolon production and genet size in the wild strawberry Fragaria vesca.

PREMISE OF THE STUDY: Clonal reproduction is often associated with polyploidy and is expected to influence polyploid establishment success, but the immediate effects of whole-genome duplication (WGD) on clonal reproduction in autopolyploids are unknown. METHODS: We used synthesized neopolyploids to assess the direct effects of WGD on stolon and plantlet production in the wild strawberry Fragaria vesca by (1) comparing absolute clonal investment between diploids and neotetraploids under high and low resource conditions in the greenhouse and (2) determining realized clonal plantlet establishment and genet spatial structure using artificial field populations comprising both cytotypes. KEY RESULTS: Neotetraploids produced fewer stolons and plantlets than diploids at slower weekly rates in the greenhouse when resources were high, resulting in lower total investment in clonal reproduction. Low resources led to smaller reductions in clonal biomass for neotetraploids and less pronounced differences between cytotypes. Comparisons between neotetraploids representing 13 independent WGD events and close diploid relatives revealed considerable variation in the response to polyploidization for some clonal traits. Field populations corroborated greenhouse results; neotetraploid genets were smaller than diploid genets, containing 28% fewer stolons and 46% fewer rooted plantlets. CONCLUSIONS: WGD significantly decreases the clonal output of neotetraploid F. vesca, which is likely attributable to slower whole-plant growth of the neotetraploids than the diploids. In natural populations, smaller neotetraploid genets could decrease the probability of polyploid establishment in this species. However, variation between separate neopolyploid lines emphasizes that the response of clonal investment to WGD may not be uniform across polyploid origins.

Life-history trade-offs promote the evolution of dioecy.

Most dioecious plants are perennial and subject to trade-offs between sexual reproduction and vegetative performance. However, these broader life-history trade-offs have not usually been incorporated into theoretical analyses of the evolution of separate sexes. One such analysis has indicated that hermaphroditism is favoured over unisexuality when female and male sex functions involve the allocation of nonoverlapping types of resources to each sex function (e.g. allocations of carbon to female function vs. allocations of nitrogen to male function). However, some dioecious plants appear to conform to this pattern of resource allocation, with different resource types allocated to female vs. male sex functions. Using an evolutionarily stable strategy approach, we show that life-history trade-offs between sexual reproduction and vegetative performance enable the evolution of unisexual phenotypes even when there are no direct resource-based trade-offs between female and male sex functions. This result might help explain the preponderance of perennial life histories among dioecious plants and why many dioecious plants with annual life histories have indeterminate growth with ongoing trade-offs between sexual reproduction and vegetative growth.

Immediate vs. evolutionary consequences of polyploidy on clonal reproduction in an autopolyploid plant.

Background and Aims: Clonal reproduction in polyploids is expected to exceed that in diploids, due to either the immediate direct effects of whole-genome duplication (WGD) or selection during establishment. The timing of polyploidy effects on clonality are largely unknown despite its hypothesized influence on polyploid success. This study tests the direction and timing of divergence in clonal traits in diploid and polyploid Chamerion angustifolium. Methods: Root bud production and biomass allocation patterns were compared between diploids and synthesized tetraploids (neotetraploids), and between neotetraploids and naturally occurring tetraploids grown in a common environment. Key Results: Neotetraploids produced more root buds and fewer sexual structures than diploids and natural tetraploids; diploids and natural tetraploids had similar root bud numbers and sexual investment. The root bud:inflorescence biomass ratio was 71 % higher in neotetraploids than in natural tetraploids. Root bud location suggests that ramet density in neotetraploid genets could be higher than in diploid genets. Conclusions: WGD immediately increases investment in asexual vs. sexual reproduction in C. angustifolium, potentially promoting within-cytotype mating and establishment for neopolyploids. However, evolutionary change after the polyploidization event negates the direct effects of WGD. Natural polyploids and diploids have similar root bud production and biomass allocation patterns, probably resulting from habitat- and ploidy-mediated selection on polyploids to become more like diploids. These results highlight the value of studying the effects of polyploidization in young vs. established polyploids.

Consequences of clonality for sexual fitness: Clonal expansion enhances fitness under spatially restricted dispersal.

Clonality is a pervasive feature of sessile organisms, but this form of asexual reproduction is thought to interfere with sexual fitness via the movement of gametes among the modules that comprise the clone. This within-clone movement of gametes is expected to reduce sexual fitness via mate limitation of male reproductive success and, in some cases, via the production of highly inbred (i.e., self-fertilized) offspring. However, clonality also results in the spatial expansion of the genetic individual (i.e., genet), and this should decrease distances gametes and sexually produced offspring must travel to avoid competing with other gametes and offspring from the same clone. The extent to which any negative effects of clonality on mating success might be offset by the positive effects of spatial expansion is poorly understood. Here, we develop spatially explicit models in which fitness was determined by the success of genets through their male and female sex functions. Our results indicate that clonality serves to increase sexual fitness when it is associated with the outward expansion of the genet. Our models further reveal that the main fitness benefit of clonal expansion might occur through the dispersal of offspring over a wider area compared with nonclonal phenotypes. We conclude that, instead of interfering with sexual reproduction, clonal expansion should often serve to enhance sexual fitness.

Trade-offs between clonal and sexual reproduction in Sagittaria latifolia (Alismataceae) scale up to affect the fitness of entire clones.

Many plants combine sexual reproduction with vegetative propagation, but how trade-offs between these reproductive modes affect fitness is poorly understood. Although such trade-offs have been demonstrated at the level of individual shoots (ramets), there is little evidence that they scale up to affect genet fitness. For hermaphrodites, reproductive investment is further divided between female and male sexual functions. Female function should generally incur greater carbon costs than male function, which might involve greater nitrogen (N) costs. Using a common garden experiment with diclinous, clonal Sagittaria latifolia we manipulated investment in reproduction through female and male sex functions of 412 plants from monoecious and dioecious populations. We detected a 1:1 trade-off between biomass investment in female function and clonal reproduction. For male function, there was no apparent trade-off between clonal and sexual reproduction in terms of biomass investment. Instead, male function incurred a substantially higher N cost. Our results indicate that: trade-offs between investment in clonal propagation and sexual reproduction occur at the genet level in S. latifolia; and sexual reproduction interferes with clonal expansion, with investment in female function limiting the quantity of clonal propagules produced, and investment in male function limiting the nutrient content of clonal propagules.