Reconstructing the history and biological consequences of a plant invasion on the Galapagos islands

Abstract

The introduction of non-native species into new habitats is one of the foremost risks to global biodiversity. Here, we evaluate a recent invasion of wild tomato (Solanum pimpinellifolium) onto the Galapagos islands from a population genomic perspective, using a large panel of novel collections from the archipelago as well as historical accessions from mainland Ecuador and Peru. We infer a recent invasion of S. pimpinellifolium on the islands, largely the result of a single event from central Ecuador which, despite its recency, has rapidly spread onto several islands in the Galapagos. By reconstructing patterns of local ancestry throughout the genomes of invasive plants, we uncover evidence for recent hybridization and introgression between S. pimpinellifolium and the closely related endemic species Solanum cheesmaniae. Two large introgressed regions overlap with known fruit color loci involved in carotenoid biosynthesis. Instead of red fruits, admixed individuals with endemic haplotypes at these loci have orange fruit colors that are typically characteristic of the endemic species. We therefore infer that introgression explains the observed trait convergence. Moreover, we infer roles for two independent loci in driving this pattern, and a likely history of selection favoring the repeated phenotypic transition from red to orange fruits. Together, our data reconstruct a complex history of invasion, expansion, and gene flow among wild tomatoes on the Galapagos islands. These findings provide critical data on the evolutionary importance of hybridization during colonization and its role in influencing conservation outcomes. Significance StatementThe isolation and unique diversity of the Galapagos Islands provide numerous natural experiments that have enriched our understanding of evolutionary biology. Here we use population genomic sequencing to reconstruct the timing, path, and consequences of a biological invasion by wild tomato onto the Galapagos. We infer that invasive populations originated from a recent human-mediated migration event from central Ecuador. Our data also indicate that invasive populations are hybridizing with endemic populations, and that this has led to some invasive individuals adopting both fruit color genes and the fruit color characteristic of the endemic island species. Our results demonstrate how hybridization can shape patterns of trait evolution over very short time scales, and characterize genetic factors underlying invasive success.