Economists know that the consumer’s taste drives variety and innovation in almost every field of industry. It is the same in the natural world. An international team of researchers has determined that just as consumers’ diverse food preferences give rise to varied menu offerings, the preferences of plant-eating insects’ play a role in maintaining and shaping the genetic variation of their host
in a geographic area.
The new study, which will appear in the journal Science, involves aphids and the small research plant Arabidopsis thaliana, commonly known as wall cress. The findings provide the first measurable evidence that the process of natural selection and genetic diversity is driven by the predator-prey relationship between insects and plants. The pressures that natural enemies exert on plants forces them to create diverse natural defenses in order to avoid being eaten. The study also found that plants were quick to abandon those defense mechanisms when pests disappeared, confirming the high costs of these defenses.
“Our data demonstrate that there is a link between the abundance of two types of aphids and the continental distribution of Arabidopsis plants that are genetically different in terms of the biochemicals they produce to defend against insect feeding,” said UC Davis botanist Dan Kliebenstein.
Kliebenstein and his colleagues are examining the naturally occurring chemicals that the plant uses to ward off potential predators. They hope to better understand the role of these biochemicals in the environment and to explore their potential for improving human nutrition and fighting cancer.
GENETIC VARIATION: THE KEY TO SURVIVAL
Genetic change and variation are crucial to allowing a plant and animal species to survive changing environmental conditions such as new diseases or pests.
The team has documented that nonbiological changes, such as soil and climate variation, can exert pressures that cause genetic changes within a plant species. Prior to this study, there was little direct evidence that biological forces like feeding insects or species competition could lead to genetic variation within a single species across a large geographic area.
The scientists mapped the distribution of six different chemical profiles within Arabidopsis thaliana plants across Europe. Each chemical profile is controlled by variations in three genes. When they mapped out the geographic distribution of these genes in Arabidopsis plants, they noticed a change in the function of one of the key genes across different geographic regions. The gene that they identified changed in plants as they were tracked from southwest to northwest.
The theory that the researchers created to explain this is that two aphid species — Brevicoryne brassicae and Lipaphis erysimi (cabbage and mustard aphids, respectively) — are most likely the cause of the geographic variation. Both aphid species are abundant in the regions and they feed heavily on Arabidopsis and other related plants.
The team examined data on fluctuations in aphid populations in Europe that was collected for nearly 50 years by British researchers. What they found was that the distribution of the two aphid species closely mirrored the geographic distribution of the different variations of Arabidosis plants. One aphid preferred the northeastern chemical type, while the other preferred the southwestern chemical type.
“There is natural variation in chemical defenses which is under genetic control,” explained ecologist Tobias ZÃ¼st from the University of Zurich. “And this variation is maintained by geographic variation in the composition of aphid communities.”
“Genetic variation is the raw material for evolution, so the maintenance of genetic diversity is essential if populations are to respond to future environmental changes such as climate change or environmental degradation”.
Next, the team attempted to determine whether the similarity between the distribution patterns of the plants and the two aphid species was more than a coincidence. To do this, they set up an experiment that allowed them to observe what would happen when the different aphid types fed on five generations of experimentally raised Arabidopsis thaliana plants.
The team confirmed that the plants were genetically adapting to the aphids. Each successive plant generation showed less damage from the insects’ feeding. The genetic changes that each generation of plant underwent were specific to the type of aphid that was feeding on them. Moreover, the laboratory plants evolved in a way that mirrored the geographic distribution of the two aphids and the types of defense chemicals used by Thaliana plants in the wild.
The team found growth speed made a difference as well. The faster-growing Arabidosis plant types fared better, while the slowest-growing plant types actually went extinct in the experiment.
“These data make it clear that even functionally similar plant-eating pests can affect the biochemical and genetic makeup of plant populations, playing a major role in shaping and refining the plant defenses in a natural community,” Kliebenstein said.
In control populations with no aphid feeding, successful genotypes from aphid populations were lost. This occurred because defense mechanisms are costly to the plant species.
“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,” explained fellow researcher Lindsey Turnbull of the University of Zurich.
Commerical research in this field could eventually lead to the development of custom seeds that are resistant to specific local pest communities, thus limiting the need for pesticides.
EVOLUTION IN A HURRY
A similar study also published in Science was conducted by the University of Toronto Mississauga (UTM) in collaboration with Cornell University, University of Montana and University of Turku in Finland. Researchers in this study found that the effect of insects on plant evolution can happen more quickly than was previously assumed, sometimes even over a single generation.
“Scientists have long hypothesized that the interaction between plants and insects has led to much of the diversity we see among plants, including crops, but until now we had limited direct experimental evidence,” says Marc Johnson, Assistant Professor in the UTM Department of Biology.
“This research fills a fundamental gap in our understanding of how natural selection by insects causes evolutionary changes in plants as they adapt, and demonstrates how rapidly these changes can happen in nature.”
The team planted evening primrose, a typically self-fertilizing plant that produces genetically identical offspring. The primroses were planted in two different plots, each containing 60 plants of 18 different genotypes.
One plot was kept free of predatory insects using the regular biweekly application of insecticide throughout the entire study period, while the other plot was left free to natural levels of insects. The plots had no other interference for five years. Each year of the study, the team counted the number and types of plants colonizing the plots and analyzed the changing frequencies of the different evening primrose genotypes and the traits associated with those genotypes.
Anurag Agrawal, professor of ecology and evolutionary biology at Cornell University, explained: “We demonstrated that when you take moths out of the environment, certain varieties of evening primrose were particularly successful. These successful varieties have genes that produce less defenses against moths.”
The study states that evolution, expressed as a change in genotype frequency over time, was observed in all plots after only a single generation. In response to insect attack or lack thereof, plant populations began to diverge significantly in as few as three to four generations. In the untreated plots, there were increases in the frequencies of genotypes associated with higher levels of toxic chemicals in the fruits, making them unpalatable to seed predator moths. Plants that flowered later in the year also increased in number since they were able to avoid most insect predators.
The findings show that evolution might be an important mechanism for changing whole ecosystems and that these changes can occur quite rapidly.
“As these plant populations evolve, their traits change and influence their interactions with insects and other plant species, which in turn may evolve adaptations to cope with those changes,” says Johnson. “The abundance and competitiveness of the plant populations is changing. Evolution can change the ecology and the function of organisms and entire ecosystems.”
THE RIPPLE EFFECT
The researchers also observed ecological changes that involved other plant and animal species in the plots when insects were removed. Competitor plants like dandelions colonized both sets of plots; however, they were more abundant in the plot without insects, reducing the number of evening primroses in that plot. According to the study, these changes were the result of the suppression of a moth caterpillar that prefers to feed on dandelions.
“What this research shows is that changes in these plant populations were not the result of genetic drift, but directly due to natural selection by insects on plants,” says Johnson. “It also demonstrates how rapidly evolutionary change can occur — not over millennia, but over years, and all around us.”
“This experimental demonstration of how rapid evolution can shape ecological interactions supports the idea that we need to understand feedbacks between evolutionary and ecological processes in order to be able to predict how communities and ecosystems will respond to change,” said Alan Tessier, a program director in the National Science Foundation´s (NSF) Directorate for Biological Sciences.
“One of the things farmers are trying to do is breed agricultural crops to be more resistant to pests,” said Agrawal. “Our study indicates that various genetic tradeoffs may make it difficult or impossible to maintain certain desired traits in plants that are bred for pest resistance.”
Primrose oil, for example, has been used medicinally for hundreds of years and the plant is beginning to gain popularity as an herbal remedy. This research could be useful to the herbal and pharmaceutical industries.
Most previous real-time experiments on evolution have been conducted with bacteria in test tubes, not in nature as this study was. The team intends to keep the experiment running as a long-term living laboratory.
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