Polyploidy in Indian paintbrush (Castilleja; orobanchaceae) species shapes but does not prevent gene flow across species boundaries

• Premise of study: A difference in chromosome numbers (ploidy variation) between species is usually considered a major barrier to gene flow. Therefore, it is surprising that little is known about whether ploidy variation, both within and among species, influences spatial patterns of interspecific hybridization. The role that polyploidy plays in structuring gene flow patterns between three co-occurring Indian paintbrush (Castilleja) species is investigated. • Methods: Reciprocal hand pollinations were performed in populations where the three species co-occur with and without variable plants (previous data tested the ancestral hybrid history of these variable plants). I measured fruit set, seed production, seed germination, and the DNA content of parent plants and 26 synthesized F1 hybrids. Data were combined with pollinator fidelity data to estimate the contribution of individual barriers to reproductive isolation. • Key results: Interspecific gene flow could occur in all directions, but barriers were weaker for conspecific vs. heterospecific crosses. Species were nearly fixed for different ploidy levels, but some deviations occurred, primarily in populations with variable plants. Interspecific gene flow could occur across ploidy levels, but it was more likely when species had the same number of chromosomes or when resulting F1 hybrids had even numbers of chromosomes. Postzygotic reproductive barriers were generally weaker than pollinator fidelity. • Conclusions: Polyploidy likely plays a large role in shaping contemporary and historical patterns of gene flow among these species. This study suggests that differences in chromosome numbers among closely related, compatible species might help structure spatial patterns of hybridization. © 2012 Botanical Society of America

Genome-material costs and functional trade-offs in the autopolyploid Solidago gigantea (giant goldenrod) series

Premise: Increased genome-material costs of N and P atoms inherent to organisms with larger genomes have been proposed to limit growth under nutrient scarcities and to promote growth under nutrient enrichments. Such responsiveness may reflect a nutrient-dependent diploid versus polyploid advantage that could have vast ecological and evolutionary implications, but direct evidence that material costs increase with ploidy level and/or influence cytotype-dependent growth, metabolic, and/or resource-use trade-offs is limited. Methods: We grew diploid, autotetraploid, and autohexaploid Solidago gigantea plants with one of four ambient or enriched N:P ratios and measured traits related to material costs, primary and secondary metabolism, and resource-use. Results: Relative to diploids, polyploids invested more N and P into cells, and tetraploids grew more with N enrichments, suggesting that material costs increase with ploidy level. Polyploids also generally exhibited strategies that could minimize material-cost constraints over both long (reduced monoploid genome size) and short (more extreme transcriptome downsizing, reduced photosynthesis rates and terpene concentrations, enhanced N-use efficiencies) evolutionary time periods. Furthermore, polyploids had lower transpiration rates but higher water-use efficiencies than diploids, both of which were more pronounced under nutrient-limiting conditions. Conclusions: N and P material costs increase with ploidy level, but material-cost constraints might be lessened by resource allocation/investment mechanisms that can also alter ecological dynamics and selection. Our results enhance mechanistic understanding of how global increases in nutrients might provide a release from material-cost constraints in polyploids that could impact ploidy (or genome-size)-specific performances, cytogeographic patterning, and multispecies community structuring

Data from: Impacts of soil nitrogen and phosphorus levels on cytotype performance of the circumboreal herb, Chamerion angustifolium: implications for polyploid establishment

Although polyploidy commonly occurs in angiosperms, not all polyploidization events lead to successful lineages, and environmental conditions could influence cytotype dynamics and polyploid success. Low soil nitrogen and/or phosphorus concentrations often limit ecosystem primary productivity, and changes in these nutrients might differentially favor some cytotypes over others, thereby influencing polyploid establishment. We grew diploid, established tetraploid, and neotetraploid Chamerion angustifolium (fireweed) in a greenhouse under low and high soil nitrogen and phosphorus conditions and different competition treatments and measured plant performance (height, biomass, flower and root-bud production) and insect damage responses. By comparing neotetraploids to established tetraploids, we were able to examine traits and responses that might directly arise from polyploidization before they are modified by natural selection and/or genetic drift. We found that (1) neopolyploids were the least likely to survive and flower and experienced the most herbivore damage regardless of nutrient conditions; (2) both neo- and established tetraploids had greater biomass and root-bud production under nutrient enriched conditions, whereas diploid biomass and root bud production was not significantly affected by nutrients; (3) intra-cytotype competition more negatively affected diploids and established tetraploids than it did neotetraploids. Following polyploidization, biomass and clonal growth might be more immediately affected by environmental nutrient availabilities than plant survival, flowering, and/or responses to herbivory, which could influence competitive dynamics. Specifically, polyploids might have competitive and colonizing advantages over diploids under nutrient enriched conditions favoring their establishment, although establishment may also depend upon the density and occurrences of other related cytotypes in a population

Investigating the effects of whole genome duplication on phenotypic plasticity: implications for the invasion success of giant goldenrod Solidago gigantea

Polyploidy commonly occurs in invasive species, and phenotypic plasticity (PP, the ability to alter one\u27s phenotype in different environments) is predicted to be enhanced in polyploids and to contribute to their invasive success. However, empirical support that increased PP is frequent in polyploids and/or confers invasive success is limited. Here, we investigated if polyploids are more pre-adapted to become invasive than diploids via the scaling of trait values and PP with ploidy level, and if post-introduction selection has led to a divergence in trait values and PP responses between native- and non-native cytotypes. We grew diploid, tetraploid (from both native North American and non-native European ranges), and hexaploid Solidago gigantea in pots outside with low, medium, and high soil nitrogen and phosphorus (NP) amendments, and measured traits related to growth, asexual reproduction, physiology, and insects/pathogen resistance. Overall, we found little evidence to suggest that polyploidy and post-introduction selection shaped mean trait and PP responses. When we compared diploids to tetraploids (as their introduction into Europe was more likely than hexaploids) we found that tetraploids had greater pathogen resistance, photosynthetic capacities, and water-use efficiencies and generally performed better under NP enrichments. Furthermore, tetraploids invested more into roots than shoots in low NP and more into shoots than roots in high NP, and this resource strategy is beneficial under variable NP conditions. Lastly, native tetraploids exhibited greater plasticity in biomass accumulation, clonal-ramet production, and water-use efficiency. Cumulatively, tetraploid S. gigantea possesses traits that might have predisposed and enabled them to become successful invaders. Our findings highlight that trait expression and invasive species dynamics are nuanced, while also providing insight into the invasion success and cyto-geographic patterning of S. gigantea that can be broadly applied to other invasive species with polyploid complexes

Data from: Adaptive molecular evolution of a defence gene in sexual but not functionally asexual evening primroses

Theory predicts that sexual reproduction provides evolutionary advantages over asexual reproduction by reducing mutational load and increasing adaptive potential. Here, we test the latter prediction in the context of plant defences against pathogens because pathogens frequently reduce plant fitness and drive the evolution of plant defences. Specifically, we ask whether sexual evening primrose plant lineages (Onagraceae) have faster rates of adaptive molecular evolution and altered gene expression of a class I chitinase, a gene implicated in defence against pathogens, than functionally asexual evening primrose lineages. We found that the ratio of amino acid to silent substitutions (Ka/Ks = 0.19 vs. 0.11 for sexual and asexual lineages, respectively), the number of sites identified to be under positive selection (four vs. zero for sexual and asexual lineages, respectively) and the expression of chitinase were all higher in sexual than in asexual lineages. Our results are congruent with the conclusion that a loss of sexual recombination and segregation in the Onagraceae negatively affects adaptive structural and potentially regulatory evolution of a plant defence protein

Genetic analysis of admixture and patterns of introgression in foundation cottonwood trees (Salicaceae) in southwestern Colorado, USA

Cottonwoods are well known as foundation riparian trees that support diverse communities and drive ecosystem processes. Although hybridization naturally occurs when the distributions of two or more cottonwood species overlap, few cottonwood hybrid zones have been genetically characterized. We use genetic and genomic analyses to characterize patterns of admixture and introgression for a newly described hybrid zone at the intersection of three species (Populus L. Salicaceae-Populus deltoides, Populus fremontii, and Populus angustifolia) in southwestern Colorado, USA. Analysis of nuclear and chloroplast microsatellite marker data detected substantial genetic variation among individuals, revealing that (1) hybridization is occurring between two, not three, species (P. deltoides and P. angustifolia); (2) gene flow is bidirectional; (3) hybrids are not abundant (admixture detected in only 34 of 270 trees), with most being early-generation F1 hybrids; (4) cytonuclear disequilibria exists and F1 hybrids tend to retain P. deltoides-like chloroplasts; and (5) roughly 30 % of the nuclear markers deviated from a neutral pattern of introgression, suggesting that selection may play a role in shaping the genetic structure of the hybrid zone in this region. Overall, our results show that despite strong selection maintaining species divergence, transfer of allelic variants across species boundaries can occur. Our study assesses the fine-scale genetic structure of hybridization between P. angustifolia and P. deltoides and lays the foundation for examining how geographic differences in hybrid zone dynamics arise and may influence subsequent ecological and evolutionary processes. © 2014 Springer-Verlag Berlin Heidelberg

Unique arthropod communities on different host-plant genotypes results in greater arthropod diversity

Studies on the effect of plant-species diversity on various ecological processes has led to the study of the effects of plant-genetic diversity in the context of community genetics. Arthropod diversity can increase with plant-species or plant-genetic diversity (Wimp et al. in Ecol Lett 7:776-780, 2004). Plant diversity effects can be difficult to separate from other ecological processes, for example, complementarity. We asked three basic questions: (1) Are arthropod communities unique on different host-plant genotypes? (2) Is arthropod diversity greater when associated with greater plant-genetic diversity? (3) Are arthropod communities more closely associated with host-plant genetics than the plant neighborhood? We studied canopy arthropods on Populus fremontii trees randomly planted in a common garden. All trees were planted in a homogeneous matrix, which helped to reduce P. fremontii neighborhood effects. One sample was comprised of few P. fremontii genotypes with many clones. A second sample was comprised of many P. fremontii genotypes with few clones. A second data set was used to examine the relationships between the arthropod community with P. fremontii genetic composition and the neighborhood composition of the focal host plant. Unique arthropod communities were associated with different P. fremontii genotypes, and arthropod community diversity was greater in the sample with greater P. fremontii genotypic diversity. Arthropod community similarity was negatively correlated with P. fremontii genetic distance, but arthropod community similarity was not related to the neighborhood of the P. fremontii host plant. © 2012 Springer Science+Business Media B.V

Landscape Resistance Models Identify Genetic Connectivity Corridors for a Foundation Riparian Tree (\u3cem\u3ePopulus angustifolia\u3c/em\u3e)

Gene flow is a fundamental evolutionary process that underlies species\u27 ability to adapt to changing environments. Yet, for most species, little is known about the specific factors that facilitate or inhibit dispersal through complex landscapes, and the effects these factors have on patterns of genetic diversity and differentiation. We applied a landscape genetic approach to understand how environment and climate influence the movement of genes in a foundation riparian tree (Populus angustifolia), and their relationships with species-wide patterns of genetic diversity and differentiation. Using multivariate restricted optimization in a reciprocal causal modeling framework, we quantified the relative contributions of river network connectivity, terrestrial uplands, and climate on genetic connectivity. We found that (1) all river orders facilitated gene flow, and terrestrial uplands provided 2.5 times more resistance than riparian corridors. (2) Cumulative differences in precipitation seasonality and precipitation of the warmest quarter were the primary climatic factors driving genetic differentiation. (3) Landscape connectivity was positively correlated with genetic diversity. Comparing our findings with a similar study of P. fremontii suggests that asexual reproduction may be a critical adaptation facilitating P. angustifolia\u27s broader distribution along headwater reaches. Both cottonwoods and other recent studies of shrubs suggest an emerging trend of the general importance of cumulative differences in precipitation gradients in driving spatial patterns of genetic differentiation. Our finding that connectivity was closely related to genetic diversity in P. angustifolia illustrates the utility of landscape resistance models for identifying factors that promote species resiliency in the face of global change

Landscape Resistance Models Identify Genetic Connectivity Corridors for a Foundation Riparian Tree (\u3cem\u3ePopulus angustifolia\u3c/em\u3e)

Gene flow is a fundamental evolutionary process that underlies species\u27 ability to adapt to changing environments. Yet, for most species, little is known about the specific factors that facilitate or inhibit dispersal through complex landscapes, and the effects these factors have on patterns of genetic diversity and differentiation. We applied a landscape genetic approach to understand how environment and climate influence the movement of genes in a foundation riparian tree (Populus angustifolia), and their relationships with species-wide patterns of genetic diversity and differentiation. Using multivariate restricted optimization in a reciprocal causal modeling framework, we quantified the relative contributions of river network connectivity, terrestrial uplands, and climate on genetic connectivity. We found that (1) all river orders facilitated gene flow, and terrestrial uplands provided 2.5 times more resistance than riparian corridors. (2) Cumulative differences in precipitation seasonality and precipitation of the warmest quarter were the primary climatic factors driving genetic differentiation. (3) Landscape connectivity was positively correlated with genetic diversity. Comparing our findings with a similar study of P. fremontii suggests that asexual reproduction may be a critical adaptation facilitating P. angustifolia\u27s broader distribution along headwater reaches. Both cottonwoods and other recent studies of shrubs suggest an emerging trend of the general importance of cumulative differences in precipitation gradients in driving spatial patterns of genetic differentiation. Our finding that connectivity was closely related to genetic diversity in P. angustifolia illustrates the utility of landscape resistance models for identifying factors that promote species resiliency in the face of global change