Introgression shapes fruit color convergence in invasive Galápagos tomato
Abstract
Invasive species represent one of the foremost risks to global biodiversity. Here, we use population genomics to evaluate the history and consequences of an invasion of wild tomato-Solanum pimpinellifolium-onto the Galápagos islands from continental South America. Using >300 archipelago and mainland collections, we infer this invasion was recent and largely the result of a single event from central Ecuador. Patterns of ancestry within the genomes of invasive plants also reveal post-colonization hybridization and introgression between S. pimpinellifolium and the closely related Galapagos endemic Solanum cheesmaniae. Of admixed invasive individuals, those that carry endemic alleles at one of two different carotenoid biosynthesis loci also have orange fruits-characteristic of the endemic species-instead of typical red S. pimpinellifolium fruits. We infer that introgression of two independent fruit color loci explains this observed trait convergence, suggesting that selection has favored repeated transitions of red to orange fruits on the Galapagos.
Data availability
Raw, demultiplexed ddRAD reads have been deposited under NCBI BioProject PRJNA661300 and will be available once processed by NCBI. Genotype files, associated datasets, and analysis scripts have been deposited on Dryad (https://doi.org/10.5061/dryad.2v6wwpzkm).Additionally, data posted to Dryad can also be accessed at https://github.com/gibsonMatt/galtom.
-
Data from: Reconstructing the history and biological consequences of a plant invasion on the Galápagos islandsDryad Digital Repository 10.5061/dryad.2v6wwpzkm.
-
Phylogenomics reveals three sources of adaptive variation during a rapid radiationDryad Digital Repository 10.5061/dryad.182dv.
-
Regional differences in the abiotic environment contribute to genomic divergence within a wild tomato speciesDryad Digital Repository 10.5061/dryad.8gtht76k4.
Article and author information
Author details
Funding
National Science Foundation (IOS 1127059)
- Leonie Moyle
Indiana University Bloomington (Brackenridge)
- Matthew JS Gibson
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2021, Gibson et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 1,961
- views
-
- 284
- downloads
-
- 10
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Ecology
- Evolutionary Biology
Eurasia has undergone substantial tectonic, geological, and climatic changes throughout the Cenozoic, primarily associated with tectonic plate collisions and a global cooling trend. The evolution of present-day biodiversity unfolded in this dynamic environment, characterised by intricate interactions of abiotic factors. However, comprehensive, large-scale reconstructions illustrating the extent of these influences are lacking. We reconstructed the evolutionary history of the freshwater fish family Nemacheilidae across Eurasia and spanning most of the Cenozoic on the base of 471 specimens representing 279 species and 37 genera plus outgroup samples. Molecular phylogeny using six genes uncovered six major clades within the family, along with numerous unresolved taxonomic issues. Dating of cladogenetic events and ancestral range estimation traced the origin of Nemacheilidae to Indochina around 48 mya. Subsequently, one branch of Nemacheilidae colonised eastern, central, and northern Asia, as well as Europe, while another branch expanded into the Burmese region, the Indian subcontinent, the Near East, and northeast Africa. These expansions were facilitated by tectonic connections, favourable climatic conditions, and orogenic processes. Conversely, aridification emerged as the primary cause of extinction events. Our study marks the first comprehensive reconstruction of the evolution of Eurasian freshwater biodiversity on a continental scale and across deep geological time.
-
- Evolutionary Biology
Gene duplication drives evolution by providing raw material for proteins with novel functions. An influential hypothesis by Ohno (1970) posits that gene duplication helps genes tolerate new mutations and thus facilitates the evolution of new phenotypes. Competing hypotheses argue that deleterious mutations will usually inactivate gene duplicates too rapidly for Ohno’s hypothesis to work. We experimentally tested Ohno’s hypothesis by evolving one or exactly two copies of a gene encoding a fluorescent protein in Escherichia coli through several rounds of mutation and selection. We analyzed the genotypic and phenotypic evolutionary dynamics of the evolving populations through high-throughput DNA sequencing, biochemical assays, and engineering of selected variants. In support of Ohno’s hypothesis, populations carrying two gene copies displayed higher mutational robustness than those carrying a single gene copy. Consequently, the double-copy populations experienced relaxed purifying selection, evolved higher phenotypic and genetic diversity, carried more mutations and accumulated combinations of key beneficial mutations earlier. However, their phenotypic evolution was not accelerated, possibly because one gene copy rapidly became inactivated by deleterious mutations. Our work provides an experimental platform to test models of evolution by gene duplication, and it supports alternatives to Ohno’s hypothesis that point to the importance of gene dosage.