Invasion at the margins: Evidence of genetic, phenotypic, and niche shifts in a widespread invader
Rapid evolutionary change is commonly observed in introduced species, which has challenged our understanding of founder effects, hybridization, genetic drift, and gene flow. Additionally, populations at the margins of range expanding species may have lower effective population sizes and lower phenotypic and genetic diversity, thus experiencing slower evolution than central populations. However, marginal populations are also hypothesized to have greater differentiation and a greater frequency of mutations and rare alleles, which may also promote local habitat specialization at range limits of colonizing species in spite of low genetic variation. In this study we investigate phenotypic variation in Johnsongrass (Sorghum halepense), and relate it to niche expansion and genetic differentiation using a broad sample representing most of the US introduced range. Johnsongrass is one of the world’s most economically and ecologically damaging invasive plants. Johnsongrass expanded from founding populations in Arizona and South Carolina and subsequently spread across most of the southern US, with projections of northward movement with climate change. In this study we grew 488 genotyped Johnsongrass accessions from 70 sites throughout the United States in two common gardens representing contrasting climates and we recorded important functional traits.
Genetic analyses revealed a five-phase invasion progression, with independent introductions in the Southeastern and Southwestern US into agricultural fields. Johnsongrass subsequently invaded agricultural and non-agricultural habitat, while lastly reinvading the founding range in disturbed habitats. Johnsongrass accessions performed best (eg, highest biomass) when the common garden climate more closely matched their home climate. Johnsongrass grew taller in the warmer garden, but had fewer smaller culms and were smaller than those in the cooler garden. Ecological niche models showed that Johnsongrass’ climatic niche shifted and expanded as it invaded the United States, with more recently derived populations colonizing colder, wetter, and more diverse climates. In keeping with the hypothesis that population divergence is highest at range margins, niche differentiation was greater in derived subpopulations at the invasion frontier than in central, ancestral populations. Our results reveal that local genetic differentiation resulted in strong and consistent phenotypic differentiation as Johnsongrass colonized the United States, and supports the hypothesis that local adaptation of nascent populations at invasion margins is important in the success of invasive species. Our results paint one of the clearest and most complete pictures to date of how invasive plant species change in form, genetics, and habitat upon introduction to a new range.