Rui‐Ting Ju

Rapid adaptive evolution is increasingly recognized as a key driver of plant invasion success. Few studies have simultaneously examined the coevolution of multidimensional traits of growth, reproduction and defence across large geographic scales in invasive plants. Using a 17‐site, 85‐family common‐garden experiment replicated in China, we combined multivariate trait comparisons, herbivore bioassays, climate–trait relationships and phenotypic selection analyses to test whether the saltmarsh grass Spartina alterniflora evolved integrated ‘invasion syndromes’ within 40 years of its introduction from the United States. We identified four distinct syndromes across all families. Overall, introduced Chinese families displayed superior, genetically based trait syndromes that simultaneously enhanced growth, fecundity and defence against two generalist herbivores relative to native US families. Across latitudes, the dominant mid‐latitude Chinese syndrome coupled the most vigorous growth with the strongest defences but was not predominant at any native collection site. Syndrome membership was predicted by provenance temperature and/or precipitation and generated measurable fitness advantages: selection favoured taller, better‐defended phenotypes that maximized both biomass and seed set. Latitudinal variation in eight traits within China further indicates adaptive tracking of climate across 2000 km of coastline. Synthesis. We concluded that since its introduction to China, Spartina has rapidly evolved an integrated ecological strategy to enhance invasiveness under climate‐driven selective pressure, which can explain why this grass became the most successful invader along the country's coast. Our findings highlight the importance of syndrome‐based approaches in understanding the evolutionary dynamics of plant invaders and provide insights to forecast their future range expansion.

Rapid adaptive evolution is increasingly recognized as a key driver of plant invasion success. Few studies have simultaneously examined the coevolution of multidimensional traits of growth, reproduction and defense across large geographic scales in invasive plants. Using a 17-site, 85-family common-garden experiment replicated in China, we combined multivariate-trait comparisons, herbivore bioassays, climatic modelling and phenotypic-selection analyses to test whether the salt-marsh grass Spartina alterniflora evolved integrated “invasion syndromes” within 40 years of its introduction from the USA. We identified four distinct syndromes across all families. Overall, introduced Chinese families displayed superior, genetic-based syndromes that simultaneously enhanced growth, fecundity and defense against two generalist herbivores relative to native US families. Across latitudes, the dominant mid-latitude Chinese syndrome coupled the most vigorous growth with the strongest defenses and was absent from the native range. Syndrome membership was predicted by provenance temperature and/or precipitation and generated measurable fitness advantages: selection gradients favored taller, better-defended phenotypes that maximized both biomass and seed set. Latitudinal clines in nine traits within China further indicate adaptive tracking of climate across 2,000 km of coastline. We concluded that since its introduction to China, Spartina has rapidly evolved an integrated ecological strategy to enhance invasiveness under climate-driven selective pressure, which can explain why this grass became the most successful invader along the country’s coast. Our findings highlight the importance of syndrome-based approaches in understanding the evolutionary dynamics of plant invaders, and provide insights to forecast their future range expansion.

While successful plant invasions often occur in novel environments, invasive species usually occupy broad niches within their native and introduced ranges. A better understanding of the process of invasion therefore requires a wide sampling of ranges, and a good knowledge of introduction history. We tested for differentiation in herbivore resistance among 128 introduced (European, North American) and native (Chinese, Japanese) populations of the invasive Japanese knotweed Reynoutria japonica in two common gardens in the native range: one in Shanghai and the other in Yunnan. In both common gardens, we found that herbivore resistance of plants from introduced populations differed from that from native populations in China but not from native populations in Japan, the putative source of introduction. Compared to native Chinese populations, plants from native Japanese populations and introduced European and North American populations had thicker leaves in both common gardens, and a lower C:N ratio but higher flavonoids content in the Shanghai garden. Variation in herbivore resistance was more strongly associated with climate of collecting sites for populations from the native range than for those from introduced ranges. Our results support the hypothesis that introduction of particularly resistant plants from Japan may have played a key role in driving biogeographic variation in herbivore resistance. Our study highlights the importance of understanding introduction history to interpret the biogeographic divergence of global plant invaders.

Summary: Many widespread invasive plant species express high phenotypic variation across novel environments, providing a unique opportunity to examine ecological and evolutionary dynamics under global change. However, studies often lack information about the origin of introduced populations, limiting our understanding of post‐introduction evolution. We assessed the responses of Reynoutria japonica from 128 populations spanning latitudinal transects in the native (China and Japan), and introduced (North America and Europe) ranges when grown in two common gardens. Plants from introduced populations differed in almost all traits from those from Chinese populations, but were similar to plants from the putative origin in Japan. Compared to Chinese populations, North American, European and Japanese populations expressed lower trait values and plasticity in most traits. However, plants from both introduced and Japanese populations expressed higher clonality and plasticity in clonality than plants from Chinese populations. Further, introduced populations expressed higher plasticity in clonality but lower plasticity in basal diameter compared to Japanese populations. Our findings emphasize the potential role of clonality and plasticity in clonality for invasion success. In addition, our study highlights the importance of comparisons to source populations within the native range to identify evolutionary responses of introduced plants to novel environments.

Aim: Plant invasions are a global problem that requires studying plants and their environmental associations across native and introduced ranges.Location: 2000 km transects in China, Europe and North America.Time Period: June 2019–July 2020.Major Taxa Studied: Japanese knotweed (Reynoutria japonica).Methods: We surveyed 150 populations of Japanese knotweed, a noxious invader of the temperate zone, along 2000 km transects in native China and the introduced ranges of Europe and North America.Results: We found that larger plants and denser populations in the introduced ranges were associated with shifts in leaf economy and chemical defences. Introduced knotweed populations had higher SLA but reduced leaf chlorophyll, lignin, C:N ratio and leaf toughness along with altered leaf tannins, flavonoids and alkaloids. We found three distinct multivariate knotweed phenotypes primarily in the introduced ranges, and two multivariate knotweed phenotypes mainly in native populations.Main Conclusions: Decreased herbivore and pathogen impacts in introduced populations and changes in environmental associations indicate that enemy release and novel habitat conditions might have driven the emergence of novel ecological strategies in this global plant invader.

Biological invasions pose a global challenge, affecting ecosystems worldwide and human societies. Knowledge of the evolutionary history of invasive species is critical to understanding their current invasion success and projecting their future spread. However, to date, few studies have addressed the evolutionary history and potential future spread of invaders simultaneously. In this study, we explored both evolutionary history and spatiotemporal dynamic patterns of the distribution of Reynoutria japonica, known as one of the world's worst plant invaders. We analysed 265 R. japonica samples from its current geographical ranges across three continents, using seven chloroplast DNA (cpDNA) markers to establish the phylogenetic relationships among extant populations. We combined these with ecological niche modelling to infer historical and more recent migration patterns and predict potential future distribution changes under climate change. Our results indicate that climate fluctuations and sea level changes likely facilitated the expansion of R. japonica from southern Japan to continental East Asia in the Pliocene, followed by a contraction in East Asian populations. In the recent Holocene, human activities have then enabled a linage of this species to spread from Japan to Europe and North America, resulting in three major global clades. Future climate scenarios suggest a northward expansion of R. japonica in Europe and North America, but shrinking habitat in China. Our study, thus, demonstrates the complex influences of historical climate‐driven migrations, human activities and future climate changes on the global distribution of an invasive species.

Many widespread invasive plant species express high phenotypic variation across novel environments, providing a unique opportunity to examine ecological and evolutionary dynamics under global change. However, biogeographical studies often lack information about the origin of introduced populations, limiting our understanding of post-introduction evolution of introduced species in the new range. Here, we assessed the responses of Reynoutria japonica from 128 populations spanning three latitudinal transects in the native ranges of China and Japan, and the introduced ranges of North America and Europe. When grown in two common gardens in the native range, plants from introduced populations in North America and Europe differed in almost all traits from those from native Chinese populations, but were similar to plants from native Japanese populations. Compared to Chinese populations, North American, European and Japanese populations expressed lower trait values and plasticity in most traits. However, plants from both introduced ranges and from Japanese populations expressed higher clonality and plasticity in clonality than plants from Chinese populations. In addition, introduced populations expressed higher plasticity in clonality but lower plasticity in basal diameter compared to Japanese populations. Our study showed heritable differences in phenotypes between plants from the native ranges of Japan and China, and those from the introduced ranges were similar to the putative source of origin in Japan. However, we found that introduced populations may have evolved higher plasticity in clonal growth. Our findings emphasize the critical role of clonality and plasticity in invasion success, demonstrating the importance of discriminating between source and non-source native populations to identify ecological and evolutionary responses of invasive plants to novel environments.

Like alien plant invasion, range expansion of native plants may threaten biodiversity and economies, rendering them native invaders. Variation in abiotic and biotic conditions across a large geographic scale greatly affects variation in traits and interactions with herbivores of native plant invaders, which is an interesting yet mostly unexplored issue. We used a common garden experiment to compare defensive/nutritional traits and palatability to generalist herbivores of 20 native (23.64° N–30.18° N) and introduced range (31.58° N–36.87° N) populations of Reynoutria japonica , which is a native invader following range expansion in China. We analyzed the relationships among herbivore pressure, climate, plant chloroplast haplotypes, leaf traits, and herbivore performance. Of the 16 variables tested, we observed range differences in 11 variables and latitudinal clines in nine variables. In general, herbivores performed better on the introduced plants than on the native plants, and better on the high‐latitude plants than on the low‐latitude plants within the introduced populations. Three key traits (leaf thickness, specific leaf area, and carbon‐to‐nitrogen [C:N] ratio) determined palatability to herbivores and were significantly associated with temperature and/or precipitation of plant provenance as well as with plant haplotypes but not with herbivore pressure. Our results revealed a causal sequence from plant‐range‐based environmental forces and genetic context to plant quality and palatability to herbivores in R. japonica . These findings suggest a post‐introduction evolution of R. japonica , which may partly explain the colonization success of this important native, but invasive plant.

Successful plant invasions are often explained by adaptation to novel environments. However, invasive species usually occupy broad niches within their native and introduced ranges. A true understanding of microevolution during invasion therefore requires a wide sampling of ranges, ideally with a knowledge of introduction history. We tested for genetic differentiation in herbivore resistance among 128 introduced (European, North American) and native (Chinese, Japanese) populations of the invasive Japanese knotweed ( Reynoutria japonica ) in two common gardens in the native range. In both common gardens, we found that the resistance traits of the introduced populations differed from most Chinese native populations but not from native populations in Japan, which are the two putative sources of introduction. Compared to Chinese populations, introduced European populations had thicker leaves in both common gardens with a lower C: N ratio but higher flavonoids content in the Shanghai garden. In the native range, variation in herbivore resistance was much more strongly associated with climate of origin than in introduced populations. Our results support that introducing particular resistance phenotypes from Japan played a key role in the invasion of knotweed into Europe and North America. Our study demonstrates how knowledge of introduction history can avoid misinterpretations of observed biogeographic divergence.

Rapid evolution contributes to plant invasion success. Previous studies have rarely considered the coevolution of multidimensional traits in invasive plants. We compared multiple traits related to growth, fecundity, and herbivore palatability of the widespread invader Spartina alterniflora in its native (US) and introduced (China) families across large geographic scales. Of 18 tested variables, ten revealed genetic-based differences between native and introduced ranges, and nine exhibited latitudinal clines within the introduced range. Introduced families compared to natives exhibited superior syndromes with larger growth, higher fecundity, and lower palatability, which were linked to provenance climates and could enhance plant competitiveness and spread. We conclude that within only 40 years since its introduction to China, Spartina has evolved an integrated ecological strategy to enhance invasiveness under climate selective pressure, making it the most successful invader along China’s coast. Our study underscores the importance of considering multivariate traits to understand plant invasion success.