Rapid changes in seed dispersal traits may modify plant responses to global change

Abstract

When climatic or environmental conditions change, plant populations must either adapt to these new conditions, or track their niche via seed dispersal. Adaptation of plants to different abiotic environments has mostly been discussed with respect to physiological and demographic parameters that allow local persistence. However, rapid modifications in response to changing environmental conditions can also affect seed dispersal, both via plant traits and via their dispersal agents. Studying such changes empirically is challenging, due to the high variability in dispersal success, resulting from environmental heterogeneity, and substantial phenotypic variability of dispersal-related traits of seeds and their dispersers. The exact mechanisms that drive rapid changes are often not well understood, but the ecological implications of these processes are essential determinants of dispersal success, and deserve more attention from ecologists, especially in the context of adaptation to global change. We outline the evidence for rapid changes in seed dispersal traits by discussing variability due to plasticity or genetics broadly, and describe the specific traits and biological systems in which variability in dispersal is being studied, before discussing some of the potential underlying mechanisms. We then address future research needs and propose a simulation model that incorporates phenotypic plasticity in seed dispersal. We close with a call to action and encourage ecologists and biologist to embrace the challenge of better understanding rapid changes in seed dispersal and their consequences for the reaction of plant populations to global change.

Figure 1.

Dispersal stages, and possibilities of their modification via rapid responses of plant dispersal traits to global environmental change. Global environmental change includes changes in temperature, precipitation, habitat availability, biodiversity and nutrient availability, which in turn can elicit rapid responses in plant traits affecting their dispersal. These responses may affect traits of the maternal plant up to seed release (Source processes), traits that directly influence the initiation of dispersal (maternal or seed traits) (Release processes) and the dispersal process itself (seed traits) (Relocation process), traits that are important after the dispersal process (seed traits) (Destination process) and might even affect the performance of the next generation (maternal and transgenerational effects) (Process stages Jongejans et al. 2015). Potential consequences of a rapid response of dispersal traits to climate change are exemplified with a study by Teller et al. (2014). They studied the effect of drought on varying dispersal traits during different stages of the dispersal process (traits with *) in Carduus nutans. Drought conditions (red figures) reduced plant and seed release height, whereas well-watered plants (blue figures) showed more variability in their height (A). Interestingly, seeds from taller C. nutans plants in the drought treatment should disperse at least as far as same-sized individuals under well-watered conditions due to a decrease in seed terminal velocity in the drought treatment (B). Under drought stress, phenotypic plasticity of maternal plant and seed traits (C) could hence favour longer distance dispersal (D) but with the cost of fewer seeds that might also germinate later (E). Maternal effects for the next generation could not be observed in this example (F). Panels (B), (E) and (F) are reproduced with permission from Teller et al. (2014).

Figure 2.

Rapid trait changes in response to environmental change (A) in relation to the eco-evolutionary timescale (B), exemplified for potential epigenetic heritability of changes in dispersal traits (C). (A) Variation of traits in a population can be caused by phenotypic plasticity of one genotype or the standing genetic variation (several genotypes). Changes in environmental conditions could trigger epigenetic responses, with the expression of a specific phenotype. Environmental changes could also select for a specific phenotype based on a specific genotype. If epigenetic effects are transgenerational, they might lead to the continuous expression of a specific phenotype, potentially affecting rapid evolution. Continuous selection for a specific trait from the standing genetic variation can lead to rapid evolution in response to changing environmental conditions. (B) For rapid trait changes, the evolutionary timescale matches the ecological timescale, i.e. trait changes happen in direct response to environmental changes. Epigenetic parental effects might affect only one or two generations, but transgenerational epigenetic effects can span multiple generations. Rapid evolution can occur over a low number of generations, for example by selection on the standing genetic variation. (C) Epigenetic effects in response to environmental changes might be heritable. In this example, epigenetics lead to the expression of a phenotype with higher dispersal ability in response to adverse environmental conditions to escape these conditions. If the epigenetic effect is heritable, the population might change towards having higher dispersal ability and hence be able to escape adverse environmental conditions better.

Figure 3.

The figure shows the spread rate of the plant species in question as a function of the plasticity parameter α. Here G₁ and G₂ represent overall survival rates associated to the two seed dispersal pathways.