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.

Exploring environmental selection on genome size in angiosperms.

Angiosperms show a remarkable range in genome size (GS), yet most species have small genomes, despite the frequency of polyploidy and repeat amplification in the ancestries of most lineages. It has been suggested that larger genomes incur costs that have driven selection for GS reduction, although the nature of these costs and how they might impact selection remain unclear. We explore potential costs of increased GS encompassing impacts on minimum cell size with consequences for photosynthesis and water-use efficiency and effects of greater nitrogen and phosphorus demands of the nucleus leading to more severe trade-offs with photosynthesis. We suggest that nutrient-, water-, and/or CO2-stressed conditions might favour species with smaller genomes, with implications for species' ecological and evolutionary dynamics.

Genetic data improves niche model discrimination and alters the direction and magnitude of climate change forecasts.

Ecological niche models (ENMs) have classically operated under the simplifying assumptions that there are no barriers to gene flow, species are genetically homogeneous (i.e., no population-specific local adaptation), and all individuals share the same niche. Yet, these assumptions are violated for most broadly distributed species. Here, we incorporate genetic data from the widespread riparian tree species narrowleaf cottonwood (Populus angustifolia) to examine whether including intraspecific genetic variation can alter model performance and predictions of climate change impacts. We found that (1) P. angustifolia is differentiated into six genetic groups across its range from México to Canada and (2) different populations occupy distinct climate niches representing unique ecotypes. Comparing model discriminatory power, (3) all genetically informed ecological niche models (gENMs) outperformed the standard species-level ENM (3-14% increase in AUC; 1-23% increase in pROC). Furthermore, (4) gENMs predicted large differences among ecotypes in both the direction and magnitude of responses to climate change and (5) revealed evidence of niche divergence, particularly for the Eastern Rocky Mountain ecotype. (6) Models also predicted progressively increasing fragmentation and decreasing overlap between ecotypes. Contact zones are often hotspots of diversity that are critical for supporting species' capacity to respond to present and future climate change, thus predicted reductions in connectivity among ecotypes is of conservation concern. We further examined the generality of our findings by comparing our model developed for a higher elevation Rocky Mountain species with a related desert riparian cottonwood, P. fremontii. Together our results suggest that incorporating intraspecific genetic information can improve model performance by addressing this important source of variance. gENMs bring an evolutionary perspective to niche modeling and provide a truly "adaptive management" approach to support conservation genetic management of species facing global change.

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

PREMISE: 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. METHODS: 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 production, 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. RESULTS: 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; and (3) intra-cytotype competition more negatively affected diploids and established tetraploids than it did neotetraploids. CONCLUSIONS: 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.

Effects of soil nitrogen on diploid advantage in fireweed, Chamerion angustifolium (Onagraceae).

In many ecosystems, plant growth and reproduction are nitrogen limited. Current and predicted increases of global reactive nitrogen could alter the ecological and evolutionary trajectories of plant populations. Nitrogen is a major component of nucleic acids and cell structures, and it has been predicted that organisms with larger genomes should require more nitrogen for growth and reproduction and be more negatively affected by nitrogen scarcities than organisms with smaller genomes. In a greenhouse experiment, we tested this hypothesis by examining whether the amount of soil nitrogen supplied differentially influenced the performance (fitness, growth, and resource allocation strategies) of diploid and autotetraploid fireweed (Chamerion angustifolium). We found that soil nitrogen levels differentially impacted cytotype performance, and in general, diploids were favored under low nitrogen conditions, but this diploid advantage disappeared under nitrogen enrichment. Specifically, when nitrogen was scarce, diploids produced more seeds and allocated more biomass toward seed production relative to investment in plant biomass or total plant nitrogen than did tetraploids. As nitrogen supplied increased, such discrepancies between cytotypes disappeared. We also found that cytotype resource allocation strategies were differentially dependent on soil nitrogen, and that whereas diploids adopted resource allocation strategies that favored current season reproduction when nitrogen was limiting and future reproduction when nitrogen was more plentiful, tetraploids adopted resource allocation strategies that favored current season reproduction under nitrogen enrichment. Together these results suggest nitrogen enrichment could differentially affect cytotype performance, which could have implications for cytotypes' ecological and evolutionary dynamics under a globally changing climate.

Conserving threatened riparian ecosystems in the American West: Precipitation gradients and river networks drive genetic connectivity and diversity in a foundation riparian tree (Populus angustifolia).

Gene flow is an evolutionary process that supports genetic connectivity and contributes to the capacity of species to adapt to environmental change. Yet, for most species, little is known about the specific environmental factors that influence genetic connectivity, or their effects on genetic diversity and differentiation. We used a landscape genetic approach to understand how geography and climate influence genetic connectivity in a foundation riparian tree (Populus angustifolia), and their relationships with specieswide patterns of genetic diversity and differentiation. Using multivariate restricted optimization in a reciprocal causal modelling framework, we quantified the relative contributions of riparian network connectivity, terrestrial upland resistance and climate gradients on genetic connectivity. We found that (i) all riparian corridors, regardless of river order, equally facilitated connectivity, while terrestrial uplands provided 2.5× more resistance to gene flow than riparian corridors. (ii) Cumulative differences in precipitation seasonality and precipitation of the warmest quarter were the primary climatic factors driving genetic differentiation; furthermore, maximum climate resistance was 45× greater than riparian resistance. (iii) Genetic diversity was positively correlated with connectivity (R2  = 0.3744, p = .0019), illustrating the utility of resistance models for identifying landscape conditions that can support a species' ability to adapt to environmental change. From these results, we present a map highlighting key genetic connectivity corridors across P. angustifolia's range that if disrupted could have long-term ecological and evolutionary consequences. Our findings provide recommendations for conservation and restoration management of threatened riparian ecosystems throughout the western USA and the high biodiversity they support.

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 F(1) 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 F(1) 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.

Community genetics: what have we accomplished and where should we be going?

Research in community genetics seeks to understand how the dynamic interplay between ecology and evolution shapes simple and complex communities and ecosystems. A community genetics perspective, however, may not be necessary or informative for all studies and systems. To better understand when and how intraspecific genetic variation and microevolution are important in community and ecosystem ecology, we suggest future research should focus on three areas: (i) determining the relative importance of intraspecific genetic variation compared with other ecological factors in mediating community and ecosystem properties; (ii) understanding the importance of microevolution in shaping ecological dynamics in multi-trophic communities; and (iii) deciphering the phenotypic and associated genetic mechanisms that drive community and ecosystem processes. Here, we identify key areas of research that will increase our understanding of the ecology and evolution of complex communities but that are currently missing in community genetics. We then suggest experiments designed to meet these current gaps.

Tangled trios?: Characterizing a hybrid zone in Castilleja (Orobanchaceae).

Hybridization and polyploidization are exceedingly important processes because both influence the ecological envelope and evolutionary trajectory of land plants. These processes are frequently invoked for Castilleja (Indian paintbrushes) as contributors to morphological and genetic novelty and as complicating factors in species delimitations. Here, we provide a detailed analysis of morphological and genetic evidence for hybridization in a well-characterized hybrid swarm involving three broadly sympatric species (C. miniata, C. rhexiifolia, C. sulphurea) in western Colorado. Field-classified hybrids are present at high frequencies at these sites and show morphological intermediacy to and segregate for chloroplast DNA haplotypes with C. rhexiifolia and C. sulphurea. Contrarily, DNA content and AFLP variation show that field-classified hybrids are not recent hybrids but a distinctive fourth taxon. Actual hybrids (plants showing admixture ≥10% for two genotypic groups) comprised 13% of our sample, with most admixture involving C. rhexiifolia, C. sulphurea, and the unknown taxon. The identity of the field-classified "hybrids" remains unknown; they either represent a stabilized hybrid species or a species with uncharacteristically high diversity for color alleles. This study highlights the importance of examining concordance and discordance between morphology, cytology, and genetic criteria to understand the complex evolutionary history of diverse groups such as Castilleja.