Dynamics of genomic change during evolutionary rescue in the seed beetle Callosobruchus maculatus

Rapid adaptation can be necessary to prevent extinction when populations are exposed to extremely marginal or stressful environments. Factors that affect the likelihood of evolutionary rescue from extinction have been identified, but much less is known about the evolutionary dynamics and genomic basis of successful evolutionary rescue, particularly in multicellular organisms. We conducted an evolve and resequence experiment to investigate the dynamics and repeatability of evolutionary rescue at the genetic level in the cowpea seed beetle, Callosobruchus maculatus, when it is experimentally shifted to a stressful host plant, lentil (Lens culinaris). Low survival (~ 1%) at the onset of the experiment caused population decline. But adaptive evolution quickly rescued the population with survival rates climbing to 69% by the F5 generation and 90% by the F10 generation. Population genomic data showed that rescue likely was caused by rapid evolutionary change at multiple loci, with many alleles fixing or nearly fixing within five generations of selection on lentil. By comparing estimates of selection across five lentil-adapted C. maculatus populations (two new sublines and three long-established lines), we found that adaptation to lentil involves a mixture of parallel and idiosyncratic evolutionary changes. Parallelism was particularly pronounced in sublines that were formed after the parent line had passed through an initial bottleneck. Overall, our results suggest that evolutionary rescue in this system is driven by very strong selection on a modest number of loci, and these results provide empirical evidence that ecological dynamics during evolutionary rescue cause distinct evolutionary trajectories and genomic signatures relative to adaptation in less stressful environments. Impact Statement Evolutionary adaptation is an ongoing process in most populations, but when populations occupy particularly stressful or marginal environments, adaptation can be necessary to prevent extinction. Adaptation that reverses demographic decline and allows for population persistence is termed evolutionary rescue. Evolutionary rescue can prevent species loss from climate change or other environmental stresses, but it can also thwart attempts to control or eradicate agricultural pests and pathogens. Many factors affect the likelihood of evolutionary rescue, but little is known about the underlying evolutionary dynamics, particularly molecular evolutionary changes in multicellular organisms. Here we use a powerful combination of experimental evolution and genomics to track the evolutionary dynamics and genomic outcomes of evolutionary rescue. We focus on the seed beetle Callosobruchus maculatus, which is both an agricultural pest and a convenient model system. We specifically examine how this species is able to persist on a novel and very poor crop host, lentil. We show that evolution in an experimental seed beetle populations increases survival on lentil from ~1% to >80% in fewer than a dozen generations. This rapid adaptive evolutionary change at the trait (i.e., phenotypic) level was associated with equally rapid evolution at the molecular level, with some gene variants (i.e., alleles) showing frequency shifts of around 30% in a single generation. In contrast to most other experimental evolution studies in multicellular organisms (particularly Drosophila fruit flies), we find that gene variants at multiple loci rapidly fix, that is, reach a frequency of 100%, during adaptation to lentil. Our results suggest that the dynamics and genetics of adaptation to severe conditions could be distinct from adaptation under more benign conditions. By comparing outcomes of adaptation across multiple lines and sublines, we show that repeated rapid adaptation at the trait level does not necessarily involve the same evolutionary changes at the molecular level. This limited parallelism was likely driven by extreme population bottlenecks caused by low survival in the early generations on lentil. Indeed, evolutionary changes in sublines formed after recovery from a common bottleneck were highly parallel. This coupling of demographic (i.e., ecological) and evolutionary changes during evolutionary rescue may therefore limit the predictability of evolution. Because colonization of novel environments may often occur after a bottleneck, our results could be of general significance for understanding patterns of parallel (and non-parallel) evolutionary change in nature.