Identifying sources of genetic variation and reconstructing invasion routes for non-native introduced species is central to understanding the circumstances under which they may evolve increased invasiveness. In this study, we used genome-wide single nucleotide polymorphisms to study the colonization history of Centaurea solstitialis in its native range in Eurasia and invasions into the Americas. We leveraged this information to pinpoint key evolutionary shifts in plant size, a focal trait associated with invasiveness in this species. Our analyses revealed clear population genomic structure of potential source populations in Eurasia, including deep differentiation of a lineage found in the southern Apennine and Balkan Peninsulas and divergence among populations in Asia, eastern Europe, and western Europe. We found strongest support for an evolutionary scenario in which western European populations were derived from an ancient admixture event between populations from eastern Europe and Asia, and subsequently served as the main genetic ‘bridgehead’ for introductions to the Americas. Introductions to California appear to be from a single source region, and multiple, independent introductions of divergent genotypes likely occurred into the Pacific Northwest. Plant size has evolved significantly at three points during range expansion, including a large size increase in the lineage responsible for the aggressive invasion of California’s interior. These results reveal a long history of colonization, admixture, and trait evolution in C. solstitialis, and suggest routes for improving evidence-based management decisions for one of the most ecologically and economically damaging invasive species in the western United States.
Non-native plants are now a pervasive feature of ecosystems across the globe1. One hypothesis for this pattern is that introduced species occupy open niches in recipient communities2,3. If true, then non-native plants should often benefit from low competition for limiting resources that define niches. Many plants have evolved larger size after introduction, consistent with increased access to limiting resources4–9. It has been difficult to test whether larger size reflects adaptation to exploit open resources, however, because vacant niches are generally challenging to identify in plants. Here we take advantage of a situation in which a highly invasive non-native plant, Centaurea solstitialis L. (yellow starthistle, hereafter ‘YST’), occupies a well-described environmental niche, wherein water is a known limiting resource10,11. We use a glasshouse common environment and climatic niche modeling to reveal that invading YST has evolved a higher-fitness life history at the expense of increased dependence on water. Critically, historical declines in resident competitors have made water more available for introduced plants11,12, demonstrating how native biodiversity declines can open niches and create opportunities for introduced species to evolve increased resource use, a potentially widespread basis for introduction success and the evolution of invasive life histories.
Studying germination in the native and non-native range of a species can provide unique insights into processes of range expansion and adaptation; however, traits related to germination have rarely been compared between native and nonnative populations. In a series of common garden experiments, we explored whether differences in the seasonality of precipitation, specifically, summer drought vs summer rain, and the amount and variation of annual and seasonal precipitation affect the germination responses of populations of an annual ruderal plant, Centaurea solstitialis, from its native range and from two non-native regions with different climates. We found that seeds from all native populations, irrespective of the precipitation seasonality of the region in which they occurred, and non-native populations from regions with dry summers displayed similarly high germination proportions and rates. In contrast, genotypes from the non-native region with predominantly summer rain exhibited much lower germination fractions and rates. Also, percent germination was strongly correlated with variation in precipitation in winter, the season that follows germination for C. solstitialis. Specifically, germination was lower for native and non-native populations experiencing greater variation in winter precipitation. This correlation, however, was greatly influenced by the non-native region with summer rain, which also exhibited the greatest variation in winter precipitation among studied regions. These results suggest that rather than general climatic patterns, the degree of risk experienced at early developmental stages could exert an important control over the germination strategy of C. solstitialis populations in both native and non-native ranges. Also, these findings reveal a largely unique germination response in C. solstitialis genotypes growing in the non-native region with summer rain and high variation in winter precipitation. Our work raises the possibility that rapid adaptive changes in germination strategies may contribute to the success of globally distributed invaders.
The natural history of introduced species is often unclear due to a lack of historical records. Even when historical information is readily available, important factors of the invasions such as genetic bottlenecks, hybridization, historical relationships among populations and adaptive changes are left unknown. In this study, we developed a set of nuclear, simple sequence repeat markers and used these to characterize the genetic diversity and population structure among native (Eurasian) and non-native (North and South American) populations of Centaurea solstitialis L., (yellow starthistle). We used these data to test hypotheses about the invasion pathways of the species that were based on historical and geographical records, and we make inferences about historical relationships among populations and demographic processes following invasion. We confirm that the center of diversity and the native range of the species is likely the eastern Mediterranean region in the vicinity of Turkey. From this region, the species likely proceeded to colonize other parts of Europe and Asia via a slow, stepwise range expansion. Spanish populations were the primary source of seed to invade South America via human-mediated events, as was evident from historical records, but populations from the eastern Mediterranean region were also important. North American populations were largely derived from South America, but had secondary contributors. We suggest that the introduction history of non-native populations from disparate parts of the native range have allowed not just one, but multiple opportunities first in South America then again in North America for the creation of novel genotypes via intraspecific hybridization. We propose that multiple intraspecific hybridization events may have created especially potent conditions for the selection of a noxious invader, and may explain differences in genetic patterns among North and South America populations, inferred differences in demographic processes, as well as morphological differences previously reported from common garden experiments.
Studying germination in the native and non‐native range of a species can provide unique insights into processes of range expansion and adaptation; however, traits related to germination have rarely been compared between native and non‐native populations. In a series of common garden experiments, we explored whether differences in the seasonality of precipitation, specifically, summer drought vs summer rain, and the amount and variation of annual and seasonal precipitation affect the germination responses of populations of an annual ruderal plant, Centaurea solstitialis, from its native range and from two non‐native regions with different climates. We found that seeds from all native populations, irrespective of the precipitation seasonality of the region in which they occurred, and non‐native populations from regions with dry summers displayed similarly high germination proportions and rates. In contrast, genotypes from the non‐native region with predominantly summer rain exhibited much lower germination fractions and rates. Also, percent germination was strongly correlated with variation in precipitation in winter, the season that follows germination for C. solstitialis. Specifically, germination was lower for native and non‐native populations experiencing greater variation in winter precipitation. This correlation, however, was greatly influenced by the non‐native region with summer rain, which also exhibited the greatest variation in winter precipitation among studied regions. These results suggest that rather than general climatic patterns, the degree of risk experienced at early developmental stages could exert an important control over the germination strategy of C. solstitialis populations in both native and non‐native ranges. Also, these findings reveal a largely unique germination response in C. solstitialis genotypes growing in the non‐native region with summer rain and high variation in winter precipitation. Our work raises the possibility that rapid adaptive changes in germination strategies may contribute to the success of globally distributed invaders.
BackgroundBiological invasions are fundamentally biogeographic processes that occur over large spatial scales. Interactions with soil microbes can have strong impacts on plant invasions, but how these interactions vary among areas where introduced species are highly invasive vs. naturalized is still unknown. In this study, we examined biogeographic variation in plant-soil microbe interactions of a globally invasive weed, Centaurea solstitialis (yellow starthistle). We addressed the following questions (1) Is Centaurea released from natural enemy pressure from soil microbes in introduced regions? and (2) Is variation in plant-soil feedbacks associated with variation in Centaurea's invasive success?Methodology/Principal FindingsWe conducted greenhouse experiments using soils and seeds collected from native Eurasian populations and introduced populations spanning North and South America where Centaurea is highly invasive and noninvasive. Soil microbes had pervasive negative effects in all regions, although the magnitude of their effect varied among regions. These patterns were not unequivocally congruent with the enemy release hypothesis. Surprisingly, we also found that Centaurea generated strong negative feedbacks in regions where it is the most invasive, while it generated neutral plant-soil feedbacks where it is noninvasive.Conclusions/SignificanceRecent studies have found reduced below-ground enemy attack and more positive plant-soil feedbacks in range-expanding plant populations, but we found increased negative effects of soil microbes in range-expanding Centaurea populations. While such negative feedbacks may limit the long-term persistence of invasive plants, such feedbacks may also contribute to the success of invasions, either by having disproportionately negative impacts on competing species, or by yielding relatively better growth in uncolonized areas that would encourage lateral spread. Enemy release from soil-borne pathogens is not sufficient to explain the success of this weed in such different regions. The biogeographic variation in soil-microbe effects indicates that different mechanisms may operate on this species in different regions, thus establishing geographic mosaics of species interactions that contribute to variation in invasion success.
Aim: We studied the novel weapons hypothesis in the context of the broadly distributed tree species Eucalyptus globulus. We evaluated the hypothesis that this Australian species would produce stronger inhibitory effects on species from its non-native range than on species from its native range. Location:We worked in four countries where this species is exotic (U.S.A., Chile, India, Portugal) and one country where it is native (Australia). Major taxa studied: Plants. Methods:We compared species composition, richness and height of plant communities in 20 paired plots underneath E. globulus individuals and open areas in two sites within its native range and each non-native region. We also compared effects of litter leachates of E. globulus on root growth of seedlings in species from Australia, Chile, the U.S.A. and India.Results: In all sites and countries, the plant community under E. globulus canopies had lower species richness than did the plant community in open areas. However, the reduction was much greater in the non-native ranges: species richness declined by an average of 51% in the eight nonnative sites versus 8% in the two native Australian sites. The root growth of 15 out of 21 species from the non-native range were highly suppressed by E. globulus litter leachates, whereas the effect of litter leachate varied from facilitation to suppression for six species native to Australia.The mean reduction in root growth for Australian plants was significantly lower than for plants from the U.S.A., Chile and India.Main conclusions: Our results show biogeographical differences in the impact of an exotic species on understorey plant communities. Consistent with the novel weapons hypothesis, our findings suggest that different adaptations of species from the native and non-native ranges to biochemical compounds produced by an exotic species may play a role in these biogeographical differences.
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