Evolution of plant defense in real time: A multigenerational field experiment

Background/Question/Methods: Theory, observations, and experiments have all implicated insect herbivores as key agents of selection on plant traits.  Yet, despite some elegant demonstrations of herbivore-imposed natural selection on plants, how plant populations respond to this selection is virtually unknown because there have been no multigenerational studies that have followed the evolutionary trajectory of plant defenses in the presence and absence of herbivores. We present results from a five year multigenerational field experiment to quantify the role of insect herbivores as selective agents on specific plant defenses in the native plant Oenothera biennis.  The abundance of insect herbivores was manipulated in 16 replicated field plots to address how insect herbivores affect: 1) the strength of natural selection and the evolutionary response of O. biennis populations over multiple generations, 2) changes in plant demographic parameters through time, and the evolutionary consequences of such demographic effects, and 3) the evolutionary trajectory of specific defensive traits (phenolics, phenology, and trichomes).  Thus, we report the results of a massive genotyping and phenotyping effort to quantify both the change in plant genotype frequencies and functional trait change over time.

Results/Conclusions: Insect herbivores had strong effects on both the population density as well as frequency of genotypes of O. biennis.  In particular, three specialist herbivores that consume the reproductive structures of the plant reduced fitness, and plants showed heritable variation for resistance.  Using genotypic measures of resistance and the observed changes in genotype frequencies, we show that plant resistance evolved rapidly during the course of the experiment.  Similarly, flowering phenology, which is critical for resistance, showed rapid and sustained evolutionary change, evolving earlier in the populations with insects suppressed.  The evolution of phenology was observed in the field and was confirmed using genotype specific estimates based on changes in plant genotype frequencies.  Finally, suppressing insects enhanced populations of plant competitors of O. biennis and this interaction result in the evolution of increased competitive ability.  Thus, overall the suppression of insect herbivores resulted in the joint evolution of susceptibility to attack and enhanced plant competitive ability.