Drought-induced trans-generational tradeoff between stress tolerance and defence: consequences for range limits?

Abstract

Areas just across species range boundaries are often stressful, but even with ample genetic variation within and among range-margin populations, adaptation towards stress tolerance across range boundaries often does not occur. Adaptive trans-generational plasticity should allow organisms to circumvent these problems for temporary range expansion; however, range boundaries often persist. To investigate this dilemma, we drought stressed a parent generation of Boechera stricta (A.Gray) A. Löve & D. Löve, a perennial wild relative of Arabidopsis, representing genetic variation within and among several low-elevation range margin populations. Boechera stricta is restricted to higher, moister elevations in temperate regions where generalist herbivores are often less common. Previous reports indicate a negative genetic correlation (genetic tradeoff) between chemical defence allocation and abiotic stress tolerance that may prevent the simultaneous evolution of defence and drought tolerance that would be needed for range expansion. In growth chamber experiments, the genetic tradeoff became undetectable among offspring sib-families whose parents had been drought treated, suggesting that the stress-induced trans-generational plasticity may circumvent the genetic tradeoff and thus enable range expansion. However, the trans-generational effects also included a conflict between plastic responses (environmental tradeoff); offspring whose parents were drought treated were more drought tolerant, but had lower levels of glucosinolate toxins that function in defence against generalist herbivores. We suggest that either the genetic or environmental tradeoff between defence allocation and stress tolerance has the potential to contribute to range limit development in upland mustards.

Keywords: Boechera stricta; chemical defence; drought tolerance; epigenetic; glucosinolate; range limit; tradeoff.

Figure 1.

Watering treatments (C = Control, D = Drought) during the basal rosette stage (A), and during reproduction (i.e. bolting) (B), as measured by water weight per flat during the parent generation. Within a flat, water was distributed evenly among pots. Drought treatments began on Day 30 post planting. All flats were weighed before each watering. A cold treatment to induce flowering was administered to all flats between Days 48 and 88 post planting. Control flats were watered every other day to maintain the weights shown, while drought-treated flats were not watered until Day 48, and then periodically after cold treatments to maintain the weights shown. All of the control flats were continued as controls during reproduction (CCs), but half of the original drought-treated flats were treated as controls during reproduction (DCs), while the other drought-treated flats continued to be drought treated (DDs).

Figure 2.

Genetic correlation between the root-to-shoot ratio and 2-hydroxy-1-methylethyl GS concentration in the parent generation (A), and in the offspring whose parents were control watered (B) or drought (DCs shown) treated (C). The trend in the parents was also observed within each population (see Fig. 3A). Data are means of sib-families, controlling as needed for unmeasured random effects among planting flats and for plant size, hence the residuals. In the offspring (B and C) sib-families from both offspring watering treatments appear in each graph.

Figure 3.

The genetic tradeoff between drought stress tolerance (measured as the root-to-shoot ratio) and GS allocation in the parent generation (Fig. 1A) was observed within each population (A—least squares best fit line for each population is shown). The genetic correlation was not caused by shoot weight, which is used in the calculation of both variables (root-to-shoot ratio and GS concentration), because there was no genetic correlation between the root-to-shoot ratio and the weight of shoot tissue used for GS analysis (B—F_{1, 57} = 0.708, P = 0.403).

Figure 4.

Drought-induced trans-generational effects on tolerance to drought (A). Tolerance was calculated from the difference in shoot size measures between drought and control treatments for each sib-family within each parent treatment group, but drought tolerance was also correlated with the shoot size measured under drought conditions (F_{1, 72 =} 81.935, P < 0.001). Effects of drought and drought-induced epigenetic effects on the concentration of 2-hydroxy-1-methylethyl GS, the most common GS (B). Error bars indicate standard errors among sib-families or among populations in the case of GSs. Data from statistical analyses are given in Table 2.

Figure 5.

Effects of parental and offspring drought treatments on root-to-shoot ratios (A), shoot biomass per water content (B) and carbon isotope ratios (C). Grey bars in all three graphs represent control offspring watering treatments and open bars represent drought treatments. For root-to-shoot ratios, data on statistical analyses are given in Table 2, otherwise see Table 3. Log (root:shoot) are residuals after controlling for flat and development. Error bars are standard errors among sib-family means.