The role of adaptive trans-generational plasticity in biological invasions of plants

Abstract

High-impact biological invasions often involve establishment and spread in disturbed, high-resource patches followed by establishment and spread in biotically or abiotically stressful areas. Evolutionary change may be required for the second phase of invasion (establishment and spread in stressful areas) to occur. When species have low genetic diversity and short selection history, within-generation phenotypic plasticity is often cited as the mechanism through which spread across multiple habitat types can occur. We show that trans-generational plasticity (TGP) can result in pre-adapted progeny that exhibit traits associated with increased fitness both in high-resource patches and in stressful conditions. In the invasive sedge, Cyperus esculentus, maternal plants growing in nutrient-poor patches can place disproportional number of propagules into nutrient-rich patches. Using the invasive annual grass, Aegilops triuncialis, we show that maternal response to soil conditions can confer greater stress tolerance in seedlings in the form of greater photosynthetic efficiency. We also show TGP for a phenological shift in a low resource environment that results in greater stress tolerance in progeny. These lines of evidence suggest that the maternal environment can have profound effects on offspring success and that TGP may play a significant role in some plant invasions.

Keywords: annual plants; competitive ability; environmental stress; inclusive fitness; maternal environmental effects; phenotypic plasticity; propagule dispersal; resource patch; seed size; spatial heterogeneity.

Figure 1

Response of Cyperus esculentus to slow-release fertilizer treatments of none, distributed uniformly, or distributed as a patch, and expressed as the mean proportion (±1 SE) of the total found in the section of the plot furthest from where tubers were sown. For the patch treatment, significantly more tubers (P < 0.01), greater tuber mass (P < 0.05) and root mass (P < 0.01) were located in the resource patch section of the plot (n = 5) compared with the other two treatments.

Figure 2

Trans-generational plasticity effects on Aegilops triuncialis phenology. (A) Effect of planted seed size of Ae. triuncialis on flowering date in generation two, flowering date = 137.99 + 0.55 × planted seed size, R² = 0.16. (B) Effect of source soil type on flowering date in generation one (means significantly different, Tukey HSD, P < 0.5). (C) Effect of source soil type on seed size in generation one (mean value significantly different, Tukey HSD, P < 0.5). Bars indicate 1 SE.

Figure 3

Effects of maternal soil environment on Aegilops triuncialis photosynthetic rates and plant size. (A) Plants grown in loam soil produced offspring with a higher photosynthetic rate (μmol CO₂/m²/s) than the same genotypes grown in serpentine soil. (B) Progeny from plants grown on serpentine soil were larger than progeny from the same genotypes grown on loam soil. Bars indicate 1 SE.