Exploring tradeoffs in hyperaccumulator ecology and evolution


Evolutionary biologists have long been fascinated by how organisms adapt to their environment. A common approach to studying adaptations is to evaluate the costs and benefits of a trait, allowing us to understand how that trait provides a fitness advantage and thus how natural selection drives its evolution. Implicit in the cost/benefit approach is the concept of evolutionary tradeoffs (Agrawal et al., 2010): in a tradeoff the genesis of a beneficial feature will incur some cost. Since organisms have many traits and there are multiple potential tradeoffs for each, much of the diversity of life may be explained by the varied ways in which such tradeoffs have driven the evolution of traits. In this issue of New Phytologist, Fones et al. (pp. 916–924) illustrate a tradeoff that may explain the evolution of the trait of zinc (Zn) hyperaccumulation by the plant Noccaea caerulescens. Hyperaccumulation is the ability of some plants to sequester certain elements, usually nickel (Ni), Zn, copper (Cu), cobalt (Co) or selenium (Se), into their aboveground tissues: often to concentrations two or three orders of magnitude greater than most other plant species (van der Ent et al., 2013). Fones et al. compare N. caerulescens to the model plant Arabidopsis thaliana to determine whether the two species respond differently to pathogen infection. They do, and Fones et al. demonstrate that this difference is tied to the ability of the hyperaccumulator to tolerate high levels of Zn. Heavy metals can cause stress that generates reactive oxygen species (ROS) that can damage cellular processes. Elevated levels of ROS also are involved in pathways that signal pathogen attack and stimulate defenses against it. Fones et al. propose that evolution of hyperaccumulation required that Noccaea evolve tolerance of high levels of ROS, and the evolution of that trait led to changes in signaling pathways that originally were involved in pathogen defense. They suggest that ROS-stimulated defenses against pathogens have been replaced by the toxicity of Zn as a pathogen defense. This tradeoff prevents what may be a costly redundancy of defenses against pathogens, so that the hyperaccumulator has essentially substituted one defense mechanism for another.

In many cases hyperaccumulation is associated with unusual soils that have elevated levels of the hyperaccumulated element (van der Ent et al., 2013), but physiological studies have shown that hyperaccumulators differ from other plants growing on those same soils by having specialized uptake, transport, sequestration and tolerance abilities (Rascio & Navari-Izzo, 2011). In the context of cost/benefit analysis, these abilities likely have costs and benefits associated with them, and a major puzzle in hyperaccumulator evolution is how their balance might have favored the evolution of hyperaccumulation. Fones et al. describe a tradeoff in which a defense based upon Zn, termed an elemental defense (see review in Boyd, 2007), evolves in place of defenses induced by the ROS signal. An exciting implication of the research by Fones et al. is that the physiological tradeoff they describe may have set the stage for evolution of hyperaccumulation by Noccaea caerulescens. Evolution of the Zn-based pathogen defense may have led to an ‘arms race’ between pathogenic bacteria and the plant. In this scenario, selection for increased metal tolerance of pathogenic bacteria and increased Zn concentration in the plant provide the evolutionary impetus for Zn hyperaccumulation. This scenario, termed defensive enhancement (Boyd, 2007) and conceptually modeled by Boyd (2012), is proposed by Fones et al. as a potential explanation for evolution of hyperaccumulation in N. caerulescens.

‘While the cost/benefit approach is intellectually appealing … as with most scientific approaches the devil is in the detail …’

While the cost/benefit approach is intellectually appealing and widely used to understand ecology and evolution, as with most scientific approaches the devil is in the detail of how we measure costs and benefits, as well as whether we have considered them all in our evolutionary accounting of fitness. Ecological networks are extremely complex: but with effort we can begin to understand possible ecological tradeoffs that may be involved. The best-explored case study of hyperaccumulator ecology is that of Se hyperaccumulation in Colorado, USA. In a series of papers from the laboratory of Elizabeth Pilon-Smits (recently reviewed by El Mehdawi & Pilon-Smits, 2012), the effects of Se hyperaccumulation on herbivores, competing plants, pollinators, endophytes and soil bacteria, and other associates have been examined. This research has shown that high levels of Se do have defensive effects, but they also impact multiple associated species in both positive and negative ways, making for a complex web of costs and benefits of Se hyperaccumulation.

As an example of this complexity, consider the effects of hyperaccumulation on soil under a perennial Se hyperaccumulator. Release of Se during decomposition will tend to enrich the surface soil under the canopy of a plant. This feature can produce a phenomenon called elemental allelopathy, in which less Se tolerant species will be less able to grow and thus a competitive advantage can accrue to the hyperaccumulator (El Mehdawi et al., 2011a). But the Pilon-Smits laboratory found that there was a positive effect of this elevated Se for some other plants: this included other hyperaccumulator species that benefited from the high Se soil (El Mehdawi et al., 2012), but also some nonaccumulator (but Se tolerant) plants had enhanced Se levels and this provided them with elemental defense against herbivory (El Mehdawi et al., 2011b). Thus the enhancement of soil Se had a negative effect on some competitors but a facilitating effect on others. Another example of ecological complexity comes from studies of biotic pollination of Se hyperaccumulators, which have elevated Se levels in their nectar. Quinn et al. (2011) found floral visitors did not discriminate against flowers with high and low Se nectar, showing no apparent pollination cost to the plant. But they did find elevated Se in bodies of pollinators and in honey made by honeybees. Ultimately, the effect of the elevated Se on the pollinators was unknown, because Se in high doses is toxic but in lower doses Se can have therapeutic activity.

These examples of Se hyperaccumulation may have relevance for the system studied by Fones et al., in part because Zn is another element that can have therapeutic effects. In fact, one of the reasons for studying Zn hyperaccumulators is to apply our knowledge of Zn uptake and storage mechanisms to produce crops that have greater concentrations of valuable nutrients such as Zn (Zhao & McGrath, 2013). Whether Zn in hyperaccumulator plants will affect associated organisms positively or negatively is likely just as complex as what has been revealed so far for Se. Ecological explorations of hyperaccumulator plants are in their infancy, but it is clear that untangling the ecological webs in which hyperaccumulators are embedded will reveal fascinating ecological and evolutionary relationships. Fones et al. have provided us with insight into the physiology of hyperaccumulators in a way that begins to shed light on evolution of this fascinating trait and set the stage for future explorations of tradeoffs in hyperaccumulator ecology and evolution.