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

Abstract

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.

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

“…angustifolium , Onagraceae) is a herbaceous perennial plant species that is widely distributed throughout much of the Northern Hemisphere. Diploid (2n = 2x = 36 chromosomes per cell) and autotetraploid (2n = 4x = 72 chromosomes per cell) cytotype races exist and although they are usually spatially distinct, mixed cytotype populations and triploid plants (2n = 3x = 54 chromosomes per cell) do occasionally occur (Mosquin, ; Mosquin and Small, ; Husband and Schemske, ; Husband and Schemske, ; Soltis et al., ; Bales and Hersch‐Green, ). For these experiments, we used seeds from diploid, established tetraploid, and neotetraploid genetic lines.…”

“…For these experiments, we used seeds from diploid, established tetraploid, and neotetraploid genetic lines. To create the genetic lines, we used diploid and tetraploid seeds that were originally collected in 2013 from the same mixed‐ploidy C. angustifolium populations near Fairbanks, Alaska (for collection details, see Bales and Hersch‐Green, ). Neopolyploid genetic lines were created by treating field‐collected diploid seeds (separate maternal diploid genotypes than the diploids used in this experiment, but these diploid seeds were also collected from the same mixed‐ploidy populations in 2013) with colchicine followed by hand‐pollination outcrosses with another neopolyploid flowering at the time (see below).…”

“…We applied nutrient treatments to dry soil prior to watering to minimize leaching from oversaturated soils, although actual soil nitrogen and phosphorus concentrations may have been lower due to plant use. The nitrogen concentrations were chosen to reflect low and high measurements of reactive soil nitrogen (NH 4 + NO 3 ; about 10–225 ppm μg N·g −1 soil; Van Cleve and Alexander, ; Gordon et al., ; Van Cleve et al., ; Yarie, ; Clein and Schimel, ; Stottlemyer et al., ; Jerabkova et al., ; Bales and Hersch‐Green, ), and the soil phosphorus concentrations were chosen to reflect the range of available phosphate (PO 4 ) in soil humus layers (about 0.5–100 ppm μg P·g −1 soil; Chapin et al., ; Dyrness et al., ; Yarie, ; Giesler et al., ; Neff et al., ; Stark, ; Hedwall et al., ) reported near our original seed collection sites in interior Alaska and similar ecosystems. We decided to keep relative nitrogen and phosphorus contributions equivalent across nutrient treatments and chose a 10:1 ratio of nitrogen to phosphorus and based the low and high treatments on reported nitrogen levels because nitrogen is more variable and phosphorus tends to occur at low concentrations in Alaskan soils (Chapin et al., ; Van Cleve and Alexander, ; Gordon et al., ; Dyrness et al., ; Van Cleve et al., ; Giesler et al., ; van der Welle et al., ; Jerabkova et al., ; Kielland et al., ).…”

“…WGD can also have maladaptive consequences for species’ fitness and evolutionary trajectories (such as resulting in an evolutionary “dead end”: Arrigo and Barker, ; Vanneste et al., ; Mayrose et al., ), and because WGD is a large‐scale mutation, it can also disrupt and/or alter gene orderings, gene expression patterns, and biochemical pathways that are responsible for physiological functioning, gamete formation, and phenotypic expression (Comai, ; Cifuentes et al., ; Song and Chen, ). While the effects of the abiotic and biotic environment on plant fitness have been well documented for diploids and established polyploid lineages (Maherali et al., ; Jamieson et al., ; Šmarda et al., ; Thompson et al., , ; Guignard et al., ; Guignard et al., ; Bales and Hersch‐Green, ), we generally do not know whether abiotic or biotic conditions affect newly formed polyploids (neopolyploids) differently than related established polyploids or diploids. Differential fitness responses to abiotic conditions could have implications for polyploid establishment success and population dynamics.…”

“…For example, organisms with larger genomes (such as polyploids) contain cells with increased nucleic acid contents and protein demands in comparison to closely related organisms with smaller genomes (such as diploids), and it has been predicted that organisms with larger genomes should be more negatively affected by nutrient limitations than organisms with smaller genomes (Lewis, ; Leitch and Bennett, ; Cavalier‐Smith, ; Hessen et al., ; Guignard et al., ). Several studies involving a wide range of organisms support these predictions (algae: Lewis, ; plants: Šmarda et al., ; Kang et al., ; Guignard et al., ; Bales and Hersch‐Green, ; snails: Neiman et al., ; Neiman et al., ; but see Mable, ; Grewell et al., ), suggesting that nutrient supplies could influence the ecological sorting of plant communities based upon genome size (Šmarda et al., ; Guignard et al., ). However, it is also possible that genome size does not significantly influence nitrogen and phosphorus requirements for synthesis because there is a trade‐off in cell size and cell number per area of tissue such that organisms with larger genomes do not have higher syntheses costs than organisms with smaller genomes (Cavalier‐Smith, ; Coate and Doyle, ).…”