ECOLOGICAL FITNESS COSTS IN A MULTIPLE HERBICIDE-RESISTANT LOLIUM RIGIDUM POPULATION

Research output: ThesisDoctoral Thesis

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Abstract

The use of herbicides to control weed populations has been an integral tool in agriculture since they were first developed over 50 years ago. The selection of genetic variability has been an inevitable consequence of herbicide use and today biotypes of nearly two hundred herbicide resistant weed species have evolved in agroecosystems, worldwide.
Theory on evolutionary biology predicts that in a herbicide free environment, herbicide-resistant individuals may exhibit an ecological disadvantage compared to herbicide-susceptible individuals (i.e., termed fitness cost). To assess the expression of fitness costs requires knowledge of which life history traits play major roles in plant fitness and how these interplay with environmental factors. Whether or not resistant plants incur fitness costs is essential information for a better understanding of the evolution of herbicide resistance and potentially for the design of proactive and reactive weed management practices that exploit differential fitness.
The present study is the first dedicated evaluation of the potential expression and magnitude of fitness costs associated with enhanced herbicide metabolism mediated by cytochrome P450 monooxygenase enzymes and an insensitive ACCase enzyme (Ile (1781) to Leu mutation). Three phenotypes were examined: herbicide-susceptible individuals (S), individuals possessing P450-based enhanced herbicide metabolism (P450), and multiple herbicide-resistant individuals possessing both resistant ACCase and enhanced P450-based metabolism (ACCase/P450). All three phenotypes were isolated from a single Lolium rigidum population (SLR31) and used in a series of comparative experiments carried out in controlled and field conditions.
Either constant temperatures or dark conditions markedly inhibited total germination and seedling emergence in seed individuals possessing the Ile (1781) to Leu mutation (ACCase/P450), compared to the S and P450 phenotypes. The light requirement for germination in the majority of individuals of the ACCase/P450 phenotype prevented high levels of fatal germination from deep burial in soil, compared to the S and P450 phenotypes. Despite fatal germination at depth, the S phenotype showed higher emergence from deep burial than both herbicide-resistant phenotypes (P450 and ACCase/P450). These results denote how manipulation of the environment may provide conditions for the expression of fitness costs and thus be potentially exploited by weed management practices.
In comparative growth experiments the P450-enhanced metabolism phenotype was found to incur a direct fitness cost. Both the P450 and ACCase/P450 phenotypes produced on average almost 20% less total biomass than the S phenotype during the vegetative stage. Reductions in biomass were driven by reduced CO2 assimilation rates. A negligible fitness cost was associated with the target site ACCase gene mutation (Ile (1781) to Leu) as no differences in growth were evident between the two resistant phenotypes.
Individuals possessing a P450-enhanced metabolism resistance mechanism showed an impaired ability to compete for resources when compared to herbicide susceptible individuals: the P450 phenotype showed a weakened ability to reduce growth of neighbouring individuals (competitive effect), and diminished growth (competitive response) under wheat competition at the vegetative and reproductive stages. The ACCase/P450 phenotype displayed a lower overall competitive effect than the S phenotype and was similar to the P450 phenotype, and reduced competitive response to wheat than the S phenotype at the reproductive stage. The results on competitive effects and responses conducted in this study also exemplify the lack of fitness costs associated with the Ile (1781) to Leu mutation of the ACCase enzyme. The underlying mechanisms and the evolutionary consequences of the competitive interactions among the S, P450 and ACCase/P450 phenotypes are discussed.
A field experiment conducted in different agroecological environments has shown a significant reduction (25%) in the frequency of the P450 phenotype after two generations, which contrasted with a 25% increase in the frequency of individuals of the S phenotype. The magnitude and dynamics of the changes in the values of the phenotypic frequencies did not correspond with those values predicted by genetic equilibrium theory. After two generations, the frequency (20%) of the multiple resistant individuals (ACCase/P450) did not differ from the original known phenotypic frequency. However, an estimation of the frequency of individuals possessing exclusively an insensitive ACCase within the ACCase/P450 phenotype revealed an increase from 2% to 10-21% among the different environmental conditions after two generations. This evidence suggests that fitness costs associated with P450-enhanced herbicide metabolism were also expressed in those multiple-resistant individuals possessing both P450- and ACCase-based resistance mechanisms (ACCase/P450).
This study provides robust evidence for the existence of fitness costs associated with a non-target site resistance mechanism endowed by cytochrome P450-enhanced herbicide metabolism in a L. rigidum population. Furthermore, the data in this study demonstrates that the magnitude of fitness costs conferred by P450 metabolism may alter the evolutionary trajectory of resistant individuals possessing this mechanism under diverse environmental conditions. It also became clear that the Ile (1781) to Leu mutation of the ACCase enzyme in L. rigidum does not confer any measurable fitness costs. The ecological and evolutionary consequences of the results of this study are discussed with emphasis on the management of herbicide resistance.
Original languageEnglish
QualificationDoctor of Philosophy
Awarding Institution
  • The University of Western Australia
Supervisors/Advisors
  • Powles, Steve, Supervisor
  • Neve, Paul, Supervisor
Award date11 May 2005
Publication statusUnpublished - 1 Mar 2005

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