A Field Experiment Demonstrating Plant Life-History Evolution and Its Eco-Evolutionary Feedback to Seed Predator Populations

Abstract

The extent to which evolutionary change occurs in a predictable manner under field conditions and how evolutionary changes feed back to influence ecological dynamics are fundamental, yet unresolved, questions. To address these issues, we established eight replicate populations of native common evening primrose (Oenothera biennis). Each population was planted with 18 genotypes in identical frequency. By tracking genotype frequencies with microsatellite DNA markers over the subsequent three years (up to three generations, ≈5,000 genotyped plants), we show rapid and consistent evolution of two heritable plant life-history traits (shorter life span and later flowering time). This rapid evolution was only partially the result of differential seed production; genotypic variation in seed germination also contributed to the observed evolutionary response. Since evening primrose genotypes exhibited heritable variation for resistance to insect herbivores, which was related to flowering time, we predicted that evolutionary changes in genotype frequencies would feed back to influence populations of a seed predator moth that specializes on O. biennis. By the conclusion of the experiment, variation in the genotypic composition among our eight replicate field populations was highly predictive of moth abundance. These results demonstrate how rapid evolution in field populations of a native plant can influence ecological interactions.

Temperature but not moisture response of germination shows phylogenetic constraints while both interact with seed mass and lifespan

“…Moreover, Agrawal et al (2013) have shown rapid evolution of life history traits in the evening primrose Oenothera biennis (Onagraceae), partly due to genotypic variation in seed germination.…”

Cryptic eco‐evolutionary dynamics

“…For instance, investigators building long-term data sets of ecological patterns could consider including measures of phenotypic, genotypic, and trait variation among the variables assayed in their study systems, and they could simultaneously attempt to set sample sizes and intervals based on the power and resolution needed to detect even transitory responses. 32,39,74,76,77 Various applications of the Price equation to such data can further assist in discerning evolution's effects from plastic and demographic influences. 72,78,79 Investigators conducting experiments can incorporate alternative genotypes or population sources in lab or field experiments 70,71,75,80 or, where actual evolution has the potential to unfold within the design, include treatments with different evolutionary potential or genotypically fixed reference conditions to estimate those effects.…”

“…A number of field studies have taken advantage of taxa or traits where it is possible to link the traits of individuals to relatively immediate ecological effects measurable at essentially the scale of those individuals or small groups of those individuals. These include studies of invertebrate and microbial dynamics on or in the vicinity of individual plants or groups of plants (i.e., foundation species 46,61,70,74 ) or of offspring contributions to population growth in pedigreed animal populations. 77,85 However, it would clearly be much more difficult to link the traits of highly vagile individuals to their respective effects on something as diffuse as a community or ecosystem response at the same time that those individuals traverse throughout open, natural systems.…”

“…Evolutionary reversals of population declines (see below) might not be apparent for generations following an initial environmental shift, but thereafter drive rapid population recovery, 50,53,54,116,117 and predator-prey interactions often involve lags such that evolution of one species might not affect responses of the other for several generations. 20,74,118 Such ecological responses to evolution might be cryptic if sampled too early or late in the process. The ability for individuals or their products (e.g., tissues, excretion, offspring) to move or be transported among systems can displace the influences of evolution to other habitats, such as when the genotypes of trees on land influence litter decomposition rates in aquatic habitats 47,119 or bear selection on salmon influences nutrient fluxes into terrestrial systems.…”

Consumer co-evolution as an important component of the eco-evolutionary feedback

“…Similarly, ecological changes have the ability to alter evolutionary dynamics and, in some cases, this can lead to reciprocal interactions between ecology and evolution, so called eco-evolutionary feedback dynamics [13][14][15] . During the last decade, the effects of ecological on evolutionary change (the eco-evo), and vice versa (the evo-eco), and in some cases reciprocal effects, have been documented in a variety of empirical systems: laboratory microcosms 10,16,17 , mesocosms and enclosures [18][19][20][21] , as well as field studies of Darwin's finches 22 , fence lizards 23 , freshwater copepods 24,25 , Soay sheep 26 and butterflies 27 . However, a demonstration of a complete feedback loop between evolutionary and ecological dynamics in a single system is still rare (but see ref.…”