Herbivorous insects, such as aphids, damage plants and can substantially reduce yields in agricultural settings; however, they can play a major role in maintaining genetic diversity. Ecologists Tobias Zust and Lindsay Turnbull from the University of Zurich together with colleagues from California and Great Britain demonstrated the importance of variation in herbivore communities using the model plant, Arabidopsis thaliana, also known as wall cress.

According to Zust, the work is one of the first experimental confirmations of a forty-year-old theory that herbivorous insects exert strong selective pressure on their host plants. Moreover, plants were quick to abandon defense mechanisms when pests were absent, confirming the high costs of these defenses.

Like many other plants, Arabidopsis thaliana, or wall cress, defends itself against pests with a sophisticated chemical arsenal. The pests, however, continually evolve mechanisms to tolerate or metabolize particular chemical components.

This means that depending on the abundance of different pest species, different compounds will provide optimal protection, and thus the plant needs to produce a carefully tailored cocktail that will be effective against the most likely attackers.

The researchers' first step was to study the distribution of different chemical defenses in natural populations of Arabidopsis thaliana across Europe and compare it to the geographic distribution of two important pest species: the cabbage and the mustard aphid.

Local pest populations as an evolutionary force
The scientists demonstrate that the main chemical compounds produced by Arabidopsis thaliana in South-western Europe differ from those in North-eastern Europe. This pattern correlates directly with a shift in the composition of the aphid communities. In the second step, the researchers studied experimentally whether different aphid species could directly select for these different chemical compounds under controlled conditions.

To this end, they exposed mixed populations of Arabidopsis thaliana to the cabbage and mustard aphid populations typical of North-eastern or South-western Europe. After five plant generations, continuous feeding by the different aphid species led to the selection of different chemical profiles, and these were consistent with the patterns seen in nature.

"There is natural variation in chemical defenses which is under genetic control", explains Zust "and this variation is maintained by geographic variation in the composition of aphid communities". "Genetic variation is the raw material for evolution", he continues, "so the maintenance of genetic diversity is essential if populations are to respond to future environmental changes such as climate change or environmental degradation".

The costs of defense
In the control populations with no aphid feeding, some of the successful genotypes from aphid populations were lost. According to Turnbull, this occurred because defense mechanisms are costly for the plant and often come at the expense of growth: "Genetic diversity was only maintained across the different treatments; within each treatment much of the diversity was lost. In the control populations, this meant the loss of defended genotypes, as here investment in costly defenses brings no benefit to the plant".

Today, the genetic diversity of many plant species is being eroded. For example, agricultural plants are selected for rapid growth and maximum yield at the expense of natural defenses, making the use of pesticides inevitable. In future, the new findings could be used to develop customized seeds that are more resistant to specific local pest communities, thus limiting the use of pesticides.

Tobias Zust, Christian Heichinger, Ueli Grossniklaus, Richard Harrington, Daniel J. Kliebenstein, Lindsay Turnbull. Natural enemies drive geographic variation in plant defenses. Science. October 5, 2012, doi: 10.1126/science.1226397.