Reconstructing the history and biological consequences of a plant invasion on the Galápagos 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 Galápagos 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 Galápagos. 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 Galápagos 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 Galápagos 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 Galápagos. 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.

Genomic signatures of admixture and selection are shared among populations of Zaprionus indianus across the western hemisphere

“…Understanding when and where admixture and local adaptation occur during the evolutionary history of introduced species is an important challenge in modern evolutionary biology. Previous work has shown how introduced species can experience admixture within their introduced range and adapt to novel environments they experience (Barker et al, 2017 ; Colautti & Barrett, 2013 ; Dlugosch & Parker, 2008 ; Gibson et al, 2020 ; Kolbe et al, 2004 ; Olazcuaga et al, 2020 ; Popovic et al, 2020 ; Simon et al, 2020 ). However, adaptations that help facilitate range expansions associated with human activities may also evolve in the invading species prior to colonization and range expansion (Hufbauer et al, 2012 ).…”

“…Genetic data are a powerful tool that can be used to estimate demographic and evolutionary events associated with introduced populations or range expansions (Barker et al, 2017 ; Bock et al, 2015 ; Dlugosch & Parker, 2008 ; Fraimout et al, 2017 ; Kolbe et al, 2004 ; Lee, 2002 ; Olazcuaga et al, 2020 ). Indeed, genetic data have been used to generate insights into biological invasions that include identifying multiple colonization events and admixture within introduced populations (Barker et al, 2017 ; Dlugosch & Parker, 2008 ; Facon et al, 2008a ; Gibson et al, 2020 ; Kolbe et al, 2004 ; Michaelides et al, 2018 ; Simon et al, 2020 ). Genome‐scale data can also be used to identify regions of the genome, and candidate genes, with evidence for selection either between native and introduced populations or among populations within species’ introduced ranges (Campbell‐Staton et al, 2020 ; Olazcuaga et al, 2020 ).…”

“…even suggest that A. sagrei's expansion in their introduced range only proceeded after genetic diversity derived from independent introductions built up within early colonizing populations in the introduced range. Recent work in other systems-introduced wild tomato (Solanum pimpinellifolium) on the Galapagos islands and introduced populations of Mytilus mussels-provide examples where admixture, or introgression, occurs either during or after species are introduced into novel environments(Gibson et al, 2020;Popovic et al, 2020;Simon et al, 2020). The dynamics of admixture in these systems, and those that we report here for Z. indianus, highlight how the timing of admixture can vary among taxa and can occur (i) during colonization and range expansion (A. sagrei and Mytilus spp.…”

Insights into invasive species from whole‐genome resequencing

“…For example, anthropogenic transport may increase opportunities for hybridization, which may then decrease the deleterious effects of a population bottleneck or increase the efficiency of adaptation This can be an affordable alternative to WGR, especially where many individual samples are required, where the species of interest has a large genome, or when a reference genome is unavailable. Successful applications of RRS (or other approaches that do not use wholegenome sequence data, such as transcriptomics) have been particularly useful when reconstructing invasion routes and inferring the demographic history of biological invasions (e.g., Gibson et al, 2020;Schmidt et al, 2020;Vallejo-Marin et al, 2021). However, RRS data are less likely to identify low-frequency alleles with shallow coalescence times compared to WGR data, and consequently may not provide sufficient resolution to estimate the timing of recent biological invasions (Part 4.1).…”

The population genomics of invasive species

“…Successful applications of reduced-representation sequencing (or other approaches that do not use whole genome sequence data, such as transcriptomics) have been particularly useful when reconstructing the evolutionary history of biological invasions (e.g. , Gibson, de Lourdes Torres, Brandvain, & Moyle, 2020;Schmidt et al, 2020). However, reduced-representation sequencing does not allow haplotype data to be used, (see Box 3), cannot identify structural variants (see Part 4), may not provide sufficient resolution to estimate the timing of recent biological invasions (Part 3), and provides limited resolution when detecting adaptation or introgression throughout the genome (Parts 4 and 5).…”