Rapid genomic and phenotypic change in response to climate warming in a widespread plant invader

Abstract

Predicting plant distributions under climate change is constrained by our limited understanding of potential rapid adaptive evolution. In an experimental evolution study with the invasive common ragweed (Ambrosia artemisiifolia L.) we subjected replicated populations of the same initial genetic composition to simulated climate warming. Pooled DNA sequencing of parental and offspring populations showed that warming populations experienced greater genetic divergence from their parents, than control populations. In a common environment, offspring from warming populations showed more convergent phenotypes in seven out of nine plant traits, with later flowering and larger biomass, than plants from control populations. For both traits, we also found a significantly higher ratio of phenotypic to genetic differentiation across generations for warming than for control populations, indicating stronger response to selection under warming conditions. As a measure for evolutionary rate, the phenotypic and sequence divergence between generations were assessed using the Haldane metric. Our approach combining comparisons between generations (allochronic) and between treatments (synchronic) in an experimental evolutionary field study, and linking population genomic data with phenotyping analyses provided a powerful test to detect rapid responses to selection. Our findings demonstrate that ragweed populations can rapidly evolve in response to climate change within a single generation. Short-term evolutionary responses to climate change may aggravate the impact of some plant invaders in the future and should be considered when making predictions about future distributions and impacts of plant invaders.

Rapid Evolution of Invasive Weeds Under Climate Change: Present Evidence and Future Research Needs

“…A. retroflexus is widespread weed of cropland and other environments throughout the world (Costea et al, 2004), and thus its apparent ability to evolve to new climatic conditions fairly rapidly (Wan et al, 2017) should be monitored closely. As mentioned previously, there is evidence for Ambrosia artemisiifolia expanding its niche breadth throughout the world (Essl et al, 2015;Gallien et al, 2016;Sun and Roderick, 2019;van Boheemen et al, 2019;Sun et al, 2020), including in China where A. artemisiifolia exhibited genetic differences in growth patterns compared to populations in North America where the species is native (Sun and Roderick, 2019; Table 1). Sun and Roderick's (2019) assessment represents evolutionary change in these Chinese populations in <100 years since the introduction of A. artemisiifolia in 1935 (Wan et al, 1993).…”

Heat wave event facilitates defensive responses in invasive C3 plant Ambrosia artemisiifolia L. under elevated CO2concentration to the detriment of insect herbivores

“…Kiesel (2014) also reported that rapid adaptation to changes in climate may in fact be key to the success of invasive plants. Recently, Sun et al (2020) demonstrated, by DNA sequencing and phenotypic observation, that common ragweed populations can rapidly evolve within a single generation in response to climate change.…”

“…It is indisputable that the concentration of CO 2 in the atmosphere will rise in the future and will increase the global temperature and drive the frequency and intensity of heat waves (Skinner et al, 2018). Previous studies have demonstrated that elevated CO 2 and warming will boost common ragweed biomass, reproduction, pollen production, and allergenic ability (Sun et al, 2020; Rogers et al, 2006; Stinson & Bazzaz, 2006; Stinson et al,2006). Sun et al (2020) also demonstrated that common ragweed populations can rapidly evolve in response to climate change within a single generation, which will aggravate the impact of its distribution and damage in the future.…”

“…Previous studies have demonstrated that elevated CO 2 and warming will boost common ragweed biomass, reproduction, pollen production, and allergenic ability (Sun et al, 2020; Rogers et al, 2006; Stinson & Bazzaz, 2006; Stinson et al,2006). Sun et al (2020) also demonstrated that common ragweed populations can rapidly evolve in response to climate change within a single generation, which will aggravate the impact of its distribution and damage in the future. Moreover, our results demonstrated that elevated CO 2 and more extreme heat events can help common ragweed improve photosynthesis, increase total leaf area, and increase growth (Supplementary Fig.1,2, and 3), which will undoubtedly increase the competitive invasion ability of this species in the future.…”

Population genomics of parallel adaptation

“…Beyond its impact on hay‐fever (allergy) and asthma sufferers, ragweed is an important agricultural weed, especially in the invaded range, and appears to have also adapted to urban environments in the USA (Gorton et al., 2018). The broad spectrum of tools in modern ecological genetics—crossing designs (McGoey et al., 2017), quantitative genetics (McGoey and Stinchcombe, 2018), manipulative experiments in the field (Gorton et al., 2019; Sun et al., 2020), genotyping by sequencing and population genetics (Martin et al., 2016; van Booheemen et al, 2017, 2018; van Boheemen & Hodgins, 2020; McGoey et al., 2020), transcriptomics (Hämälä et al., 2020)—is available in an annual plant that is of agricultural and health importance (Montagnani et al., 2017), and with a rich history of ecological investigation (e.g. MacDonald & Kotanen, 2010).…”