Comparing genetic diversity, genetic differentiation, and performance between native and nonnative populations has advanced our knowledge of contemporary evolution and its ecological consequences. However, such between‐range comparisons can be complicated by high among‐population variation within native and nonnative ranges. For example, native vs. nonnative comparisons between small and non‐representative subsets of populations for species with very large distributions have the potential to mislead because they may not sufficiently account for within‐range adaptation to climatic conditions, and demographic history that may lead to non‐adaptive evolution. We used the cosmopolitan weed Conyza canadensis to study the interplay of adaptive and demographic processes across, to our knowledge, the broadest climatic gradient yet investigated in this context. To examine the distribution of genetic diversity, we genotyped 26 native and 26 nonnative populations at 12 microsatellite loci. Furthermore, we recorded performance traits for 12 native and 13 nonnative populations in the field and in the common garden. To analyze how performance was related to range and/or climate, we fit pedigree mixed‐effects models. These models weighed the population random effect for co‐ancestry to account for the influence of demographic history on phenotypic among‐population differentiation. Genetic diversity was very low, selfing rates were very high, and both were comparable between native and nonnative ranges. Nonnative populations out‐performed native populations in the field. However, our most salient result was that both neutral genetic differentiation and common garden performance were far more correlated with the climatic conditions from which populations originated than native vs. nonnative range affiliation. Including co‐ancestry of our populations in our models greatly increased explained variance and our ability to detect significant main effects for among‐population variation in performance. High propagule pressure and high selfing rates, in concert with the ability to adapt rapidly to climatic gradients, may have facilitated the global success of this weed. Neither native nor nonnative populations were homogeneous groups but responded comparably to similar environments in each range. We suggest that studies of contemporary evolution should consider widely distributed and genotyped populations to disentangle native vs. nonnative range effects from varying adaptive processes within ranges and from potentially confounding effects of demographic history.
Summary Optimal defence allocation theory (ODT) is one of the most prominent theoretical frameworks to explain the allocation of defence compounds within plants. It predicts that the most valuable and vulnerable plant organs have the highest levels of chemical defence. The ODT has been well worked out and experimentally tested for shoot defences, but not for root defences. To assess if ODT principles apply similarly to roots and shoots, we examined glucosinolates in above‐ground and below‐ground organs of nine plant species belonging to two families. In order to evaluate whether ODT equally applies to shoot and root organs, we designed a conceptual model in which above‐ground and below‐ground organs were assigned to orders of importance to plant performance. We hypothesized that organs constituting the plant's core structure are better protected than more distal organs. The nine plant species were cultivated, and their roots and shoots were harvested and divided into three orders for glucosinolate analysis. Using a specialist (Delia radicum) and a generalist (Amphimallon solstitiale) root herbivore, we also experimentally tested the hypothesis that the generalist herbivore prefers to feed on fine roots (FRs) with a low glucosinolate concentration, while the specialist prefers taproots (TRs) with a high glucosinolate concentration. We found that both in roots and shoots, the higher ordered core structural organs (TRs and stems) had the highest levels of glucosinolates. Below‐ground, TRs and lateral roots were better protected than the more distal, and less costly, FRs in seven out of nine species tested. The specialist root herbivore preferred feeding on the highly defended TRs, which is in line with what has been found for above‐ground specialist herbivores. Moreover, the glucosinolate concentration in roots overall was significantly higher than that in shoots. Synthesis. These results support the hypothesis that Optimal defence allocation theory (ODT) generally applies to glucosinolate allocation in above‐ground and below‐ground organs and may mainly serve to maintain the integrity of the main plant structure. Moreover, it suggests that above‐ground and below‐ground insect herbivores independently exert similar selection pressures on defence allocation patterns in roots and shoots.
Herbivore‐induced defences in plants are considered a strategy to manage multiple interactions while saving resources. The optimal defence theory (ODT) is one of the most prominent theoretical frameworks to explain the defence allocation patterns within plants. It was recently shown that the ODT generally applies to constitutive glucosinolate (GSL) allocation in shoot and root organs. Previous studies showed that both root and shoot herbivore feeding may alter defence allocation over plant organs. For shoots, the effect depends on where the herbivores feed. It is as yet unknown whether similar principles apply to root‐herbivore‐induced GSLs. To analyse the effects of root localized herbivore feeding on GSL allocation, we conducted a pot experiment using Anomala cuprea grubs and four Brassicaceae; Brassica rapa, B. nigra, B. oleracea and Sinapis alba. Individuals of these four plant species were grown in dedicated mesocosms. The grubs were confined either to the bottom soil, the middle section or the topsoil. Plants grown in the same set‐ups but without root herbivores served as controls. Glucosinolate levels of the leaf lamina, petiole and stem as well as of the taproot, lateral roots and fine roots were measured after 8 days of herbivory. Plant biomass reduction due to herbivory was the largest when herbivores were confined to the topsoil. In the three Brassica species, taproot GSL levels increased upon herbivory independent of where the root herbivores were feeding. Glucosinolate levels in fine roots and shoots, on the other hand, hardly responded to root herbivory. Indole GSLs, which are more effective to pathogens than to herbivores, were more strongly induced than aliphatic and aromatic GSLs, especially in the taproots. Sinapis alba did not show remarkable increments in any GSL level upon herbivory. These results show that locally and systemically induced defences in roots are consistent with the ODT: The taproot which is the most vulnerable and valuable to plant performance shows the highest increase in defence induction. The induced GSL profiles suggest that the response may not only target herbivores, but may also help to prevent secondary infection by microbial pathogens. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13147/suppinfo is available for this article.
The optimal defense theory predicts that plants invest most energy in those tissues that have the highest value, but are most vulnerable to attacks. In Brassica species, root-herbivory leads to the accumulation of glucosinolates (GSLs) in the taproot, the most valuable belowground plant organ. Accumulation of GSLs can result from local biosynthesis in response to herbivory. In addition, transport from distal tissues by specialized GSL transporter proteins can play a role as well. GSL biosynthesis and transport are both inducible, but the role these processes play in GSL accumulation during root-herbivory is not yet clear. To address this issue, we performed two time-series experiments to study the dynamics of transport and biosynthesis in local and distal tissues of Brassica rapa. We exposed roots of B. rapa to herbivory by the specialist root herbivore Delia radicum for 7 days. During this period, we sampled above-and belowground plant organs 12 h, 24 h, 3 days and 7 days after the start of herbivory. Next, we measured the quantity and composition of GSL profiles together with the expression of genes involved in GSL biosynthesis and transport. We found that both benzyl and indole GSLs accumulate in the taproot during root-herbivory, whereas we did not observe any changes in aliphatic GSL levels. The rise in indole GSL levels coincided with increased local expression of biosynthesis and transporter genes, which suggest that both biosynthesis and GSL transport play a role in the accumulation of GSLs during root herbivory. However, we did not observe a decrease in GSL levels in distal tissues. We therefore hypothesize that GSL transporters help to retain GSLs in the taproot during root-herbivory.
Aims Plants with precise root foraging patterns can proliferate roots preferentially in nutrient-rich soil patches. When nutrients are distributed heterogeneously, this trait is often competitively advantageous in pot experiments but not field experiments. We hypothesized that this difference is due to belowground herbivory under field conditions. Methods We performed pot experiments using seedlings of Lolium perenne (a more precise root foraging species) and Plantago lanceolata (a less precise root foraging species). The experiment had a two-way factorial randomized block design, with nutrient distribution pattern (homogeneous or heterogeneous) and belowground herbivore (present or absent) as the two factors. Each pot contained one seedling of each species. Results With no herbivore present, plant biomass was smaller in the heterogeneous nutrient treatment than in the homogeneous treatment in P. lanceolata, but not in L. perenne. Under homogeneous nutrient distribution, plant biomass was lower in both species with a herbivore present than with no herbivore. Under heterogeneous nutrient distribution, biomass reduction due to herbivory occurred only in L. perenne. Conclusions Roots of the precise root foraging species were grazed more under the heterogeneous nutrient distribution, suggesting that the herbivore more efficiently foraged for roots in nutrient-rich soil patches.
We examined how the volume and temporal heterogeneity of water supply changed the vertical distribution and mortality of a belowground herbivore, and consequently affected plant biomass. Plantago lanceolata (Plantaginaceae) seedlings were grown at one per pot under different combinations of water volume (large or small volume) and heterogeneity (homogeneous water conditions, watered every day; heterogeneous conditions, watered every 4 days) in the presence or absence of a larva of the belowground herbivorous insect, Anomala cuprea (Coleoptera: Scarabaeidae). The larva was confined in different vertical distributions to top feeding zone (top treatment), middle feeding zone (middle treatment), or bottom feeding zone (bottom treatment); alternatively no larva was introduced (control treatment) or larval movement was not confined (free treatment). Three-way interaction between water volume, heterogeneity, and the herbivore significantly affected plant biomass. With a large water volume, plant biomass was lower in free treatment than in control treatment regardless of heterogeneity. Plant biomass in free treatment was as low as in top treatment. With a small water volume and in free treatment, plant biomass was low (similar to that under top treatment) under homogeneous water conditions but high under heterogeneous ones (similar to that under middle or bottom treatment). Therefore, there was little effect of belowground herbivory on plant growth under heterogeneous water conditions. In other watering regimes, herbivores would be distributed in the shallow soil and reduced root biomass. Herbivore mortality was high with homogeneous application of a large volume or heterogeneous application of a small water volume. Under the large water volume, plant biomass was high in pots in which the herbivore had died. Thus, the combinations of water volume and heterogeneity affected plant growth via the change of a belowground herbivore.
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