Resurrecting urban sunflowers: Phenotypic and molecular changes between antecedent and modern populations separated by 36 years

Abstract

Resurrection experiments provide a unique opportunity to evaluate phenotypic and molecular evolution in response to environmental challenges. To understand the evolution of urban populations of Helianthus annuus, we compared plants from 36-year-old antecedent seed collections to modern seed collections from the same area using molecular and quantitative genetic approaches. We found 200 differentially expressed transcripts between antecedent and modern groups, and transcript expression was generally higher in modern samples as compared to antecedent samples. Admixture analysis indicated gene flow from domesticated to modern populations over time. After a greenhouse refresher generation, one antecedent–modern population pair was grown under two water availability (well-watered and drought) and temperature (ambient and elevated by 2.8°C) conditions reflecting historical and contemporary climates. Overall, 78% (7 out of 9) of traits differed between the antecedent and modern populations, with modern individuals displaying some trait changes that are coherent with climate changes expectations and some trait changes in the direction of crop varieties. Phenotypic selection analysis showed that modern trait values were often favoured by selection, especially in environmental treatments resembling modern conditions. Trait heritability in the antecedent population was five times as high as in the modern population, on average. In addition, phenotypic plasticity for some traits, such as flowering phenology, was present in the antecedent population but absent in the modern population. The combination of phenotypic and molecular information suggests that evolution has been influenced by crop-wild introgression, adaptive processes and drift. We discuss these results in the context of continued evolution in response to anthropogenic factors.