In Insights we discover the story behind and beyond a recent publication in Functional Ecology. What inspired the authors to do the research, how did the project develop and what implications might their results have on the scientific community and on society?
This week, Kimberley Simpson of the Department of Animal and Plant Sciences at the University of Sheffield will provide some more detail on her paper on the implication of selection plant trade-offs.
Can you briefly explain your field of expertise, and why it is important?
I would describe myself as a plant functional ecologist primarily, but I also do some phylogenetics and physiology on the side. I’m interested in how the vast phenotypic diversity we see in the world’s flora is created and maintained by different processes. In this paper, we were investigating the effect of an artificial process (domestication/agronomic selection) on plant traits, but I’ve also studied how natural processes, such as fire, have done the same in other work. Plant traits are important drivers of ecosystem functioning (and therefore ecosystem services), and so understanding how selection shapes plant traits is important in predicting future changes to function resulting from climate and land-use change.
Can you give a brief summary of the paper?
When humans domesticated wild plants thousands of years ago, they caused these plants to change in desirable ways, such as increased yield and faster growth. These changes have continued to occur through modern breeding, and are very obvious when you compare today’s crops with their wild relatives (see image!) However, such changes may have come at a price to the plant because less of their energy is available to invest in other things, such as defences against herbivores.
Here, we investigated how domestication and modern breeding have affected defences in cereals, which include many important crops such as maize, rice and wheat. The main defence in these plants is silicon, which takes the form of spines and sharp granules in leaves, making them harder to chew and digest. We compared silicon levels of domesticated cereals with their wild ancestors and modern cultivars and found that domestication had caused a small reduction in silicon defences, but modern breeding had produced no further reduction. We also compared the amount of distasteful phenolic compounds in leaves, another defence, and found it was unchanged.
We didn’t find that crops were growing faster than their wild counterparts, as we expected from a reallocation of resources away from defence and towards growth. We did however show that plants with higher silicon levels reached a smaller size than low silicon plants, suggesting this defence is costly.
Our finding of only a small decrease in silicon through domestication suggests that cereals haven’t been disarmed by domestication: crops are as well defended as their wild ancestors.
In your paper, you show a trade-off between silicon and phenolic-based defence. Can you place these results in light of the plant economic spectrum?
The species involved in this study, being crops and their relatives, all sit at the fast end of the plant economic spectrum (fast growth, low longevity, etc.). However the trade-off we found between silicon- and carbon-based defence is consistent with the suggestion that these defences can be substituted for each other. The type of defence being deployed may depend upon a number of environmental factors, although the identification of factors which are important in determining which defence is favoured is still being explored. When carbon isn’t limiting, silicon may be a metabolically cheaper alternative to carbon in short-lived, fast-growing leaves. When carbon, and growth, is limiting, silicon may be a substitute for carbon-based defences.
What new knowledge gaps did your research expose?
The significant, but small, 10% reduction in leaf silicon we found through cereal domestication suggests that landraces may be more susceptible to herbivory than their wild progenitors. However, whether such changes in silicon are sufficient to influence herbivore behavior remains unclear. Other studies that have demonstrated impacts on herbivore preference and performance have involved much larger (>140%) changes in silicon concentration. It would be interesting to explore how the change in silicon through domestication directly impacts upon herbivore behaviour.
In your concluding remarks, you mention that silicon is potentially a way forward in improving sustainability of future agronomical practices as high silicon levels might not require high levels of pest control. How would you see such agronomical practice to role out?
Silicon addition has been used in agriculture as a way to increase yields, reduce losses to pests and pathogens and improve resilience to abiotic stress such as drought. It can be applied as natural silicates from either silica rich materials such as rice straw, or as inorganic silicates from sources such as slag from blast furnaces (a waste product of the steel industry consisting of calcium silicate). As yet there have been relatively few experimental field trials of this approach, but some studies have demonstrated significant benefits.
How do your findings translate to other ecological research disciplines?
The concept of trade-offs is central to many aspects of functional and evolutionary ecology, but finding evidence for their existence experimentally is often very difficult. We based our predictions here on the well established, but often elusive, growth-defence trade-off, but failed to find direct evidence for it. However, when we explored the data further and considered it in the context of the methodology used, we uncovered a predicted cost of silicon-based defences and a potential reason why we failed to find a growth-defence trade-off. Through our modelling approach, we found that the adverse effect of allocation to silicon defences on growth rate increases with plant size, implying that the costs of silicon defences are relatively greater for larger plants. This could be due to the greater costs of uptake, mobilization and deposition of silicon in larger plants, or because plants with higher potential maximal growth rate and final size suffer most from the costs associated with silicon uptake. Whilst we did not find a negative relationship between size-standardised growth rate (SGR) and silicon concentration, this could be due to the low common mass at which SGR values were extracted which is possibly too small to show any effects of silicon on growth rate.
Crop systems can provide a valuable system for studying ecology. Domestication, for example, provides an interesting model for looking at how rapid changes in the environment cause evolutionary change. Conversely ecological principles may have a lot to teach us about our crop plants – how were they domesticated, and why did we domesticate those certain species?
What would be your advice/message to policy makers based on your results?
Our finding that crop wild progenitors have higher defence levels (albeit to a limited extent), suggests that they may be (and already are in some cases) an important source of genetic diversity that may be used in improving the anti-herbivore defences of crops. Therefore investing in the preservation of these species is vital to future crop breeding programmes and sustainable food production. There are already a number of excellent projects attempting this, such as Kew Garden’s Crop Wild Relatives project and the Svalbard Seed Vault, so continued investment in such schemes is crucial.
As a final question, a bit more of a personal one. If you are not at work, researching grass traits, what do you like to do?
I like to be outdoors! Trail running, hiking and gardening are my favourite things to do. In Sheffield, we’re spoilt by having the Peak District National Park on our doorstep. Lots of beautiful places to explore and amazing wildlife to see. Oh, and plenty of excellent country pubs with great Yorkshire ales on tap!