Robert I. Colautti (@ColauttiLab), Queen’s University in Canada, discusses his article: Direct and indirect fitness effects of plant metabolites and genetic constraints limit evolution of allelopathy in an invading plant
A storied history
As a relatively young discipline, invasion ecology has developed through a proliferation of hypotheses that often fail to hold against careful experimentation. Model systems can be particularly valuable for exposing false hypotheses in invasion biology, for which the biennial Brassicaceae Alliaria petiolata (garlic mustard) offers a demonstrative case study.
Building on a published genome and natural accessions from across Europe and North America, our long-term goal was to map the genetic loci for a trait in A. petiolata that was widely thought to be responsible for its invasion in North America. Instead, our experiments led us to question two decades of published research linking glucosinolate production to allelopathy (i.e., competitor suppression) and invasive spread.
A model system for ‘novel weapons’?
Alliaria petiolata has been a poster child for allelopathy and the ‘Novel Weapons Hypothesis’, which attributes invasive spread to certain chemical traits that act as ‘novel weapons’ to suppress competition. It’s a compelling metaphor that complements Darwin’s ‘struggle for survival’, invoking images of military innovations that shifted the balance of power throughout the long history of human civilization. However, two decades of research have produced few compelling experiments supporting the role of allelopathy and novel weapons in invasion.
A previous study had reported that growing a single seedling of A. petiolata in a small pot of field soil was sufficient to eliminate germination of soil arbuscular mycorrhizae (AMF) and prevent mycorrhizal colonization of roots of native Acer saccharum (sugar maple) saplings, reducing plant biomass by more than 75%. A follow-up study found that the suppressive effects were much stronger on North American soil microbes than those from the native range in Europe, supporting the Novel Weapons Hypothesis. This was followed by a space-for-time analysis of herbarium records suggesting that older populations had lower glucosinolate concentrations than younger populations, consistent with eco-evolutionary feedbacks in response to native AMF evolving resistance and higher rates of intraspecific competition in expanding populations of A. petiolata.
A genetic screen for allelopathy
Motivated by these results, we designed a glasshouse and field experiment to assess genetic variation for glucosinolate concentration in 22 accessions of A. petiolata across North America. We also measured natural selection and quantified the fitness impacts of intraspecific and interspecific competition. By taking advantage of natural genetic variation, our long-term goal was to create recombinant lines to map regions of the genome associated with glucosinolate production and competitive ability. Instead, our results could not have been more inconsistent with the rapid evolution of glucosinolates as allelopathic weapons. First, A. saccharum saplings grew well in the pots containing live A. petiolata, in stark contrast to previous reports that A. petiolata is toxic to AMF. Second, glucosinolate concentrations were highly plastic across treatments, and positively correlated with chlorophyl a (Chl a) content. Third, genetic families that invested less into Chl a and more into glucosinolates were weaker competitors regardless of competition treatment (i.e., intraspecific and interspecific).
No evidence for novel weapons
Overall, our results force us to reject the idea that glucosinolates have important allelopathic properties via AMF suppression. Instead, our findings are more consistent with the well-established role of glucosinolates as defensive traits. An important advantage of model systems is that they bring together different researchers with different backgrounds, biases and expertise. Model systems force accountability and can help to distinguish ecological complexity from scientific irreproducibility.
