A test of Darwin's naturalization hypothesis in the thistle tribe shows that close relatives make bad neighbors

Invasive species have great ecological and economic impacts and are difficult to control once established, making the ability to understand and predict invasive behavior highly desirable. Preemptive measures to prevent potential invasive species from reaching new habitats are the most economically and environmentally efficient form of management. Darwin’s naturalization hypothesis predicts that invaders less related to native flora are more likely to be successful than those that are closely related to natives. Here we test this hypothesis, using the weed-rich thistle tribe, Cardueae, in the California Floristic Province, a biodiversity hotspot, as our study system. An exhaustive molecular phylogenetic approach was used, generating and examining more than 100,000 likely phylogenies of the tribe based on nuclear and chloroplast DNA markers, representing the most in-depth reconstruction of the clade to date. Branch lengths separating invasive and noninvasive introduced taxa from native California taxa were used to represent phylogenetic distances between these groups and were compared at multiple biogeographical scales to ascertain whether invasive thistles are more or less closely related to natives than noninvasive introduced thistles are. Patterns within this highly supported clade show that not only are introduced thistles more closely related to natives more likely to be invasive, but these invasive species are also evolutionarily closer to native flora than by chance. This suggests that preadaptive traits are important in determining an invader’s success. Such rigorous molecular phylogenetic analyses may prove a fruitful means for furthering our understanding of biological invasions and developing predictive frameworks for screening potential invasive taxa.Spread beyond their native ranges, some species have become numerically and ecologically dominant in new regions (1) and become of great interest and concern to scientists, policymakers, and the public. Such invasive species, sensu Colautti and MacIsaac (2), affect biodiversity, ecosystem function, and human health (3) and have ecological and economic impacts that cannot be ignored (4, 5), making the ability to understand and predict the invasiveness of species of great importance. Also, once exotic species become established in a new region, they are often extremely difficult to control (6, 7). Identifying and preventing new potentially invasive exotic species from reaching ground zero is, by far, the most economically and environmentally efficient management method (8). Hence, there is great need for early warning systems to determine the probability that a given species will become invasive (9–12).The number of plant species introduced into the United States far exceeds that of other groups of organisms (13). However, although many case studies have illuminated various aspects of plant invasions (14–22), it has proven difficult to quantify and/or make generalizations about traits, characteristics, and circumstances that contribute to plant invasiveness across multiple geographic scales and ecological systems (10, 23–28). The difficulty of devising a framework to predict the behavior of exotic plants following dislocation and the challenges of designing effective control strategies for the ones that have become invasive result from the uniqueness of the organisms involved in each case, as well as the complexity of interactions between invaders and native communities (29). Few studies have provided a practical means of addressing these issues (30, 31).Quantifiable measures that can provide robust predictions are therefore required (32), and phylogenetic relationships between native and introduced taxa may reveal patterns that invoke testable hypotheses that could not be derived from examining species traits alone (33). Distinct sets of traits evolve in response to environmental conditions, which in turn reflect past and present selection pressures and are therefore expected to differ not only among geographic regions and local communities (34), but also among evolutionary lineages. Hence species’ responses are not statistically independent from their shared evolutionary histories (35–37), and phylogeny may affect a species’ biotic interactions when it is introduced to a novel environment (38). As Darwin (39) observed, this results in a link between the evolutionary relatedness of organisms in a community, their characteristics, and the ecological processes that determine their distributions and abundance. Darwin’s naturalization hypothesis posits that invaders that are closely related to native taxa are less likely to be successful than those that are not. Assuming evolutionary relatedness is correlated with ecological similarity, such a pattern might emerge as a result of niche overlap and competitive exclusion between introduced taxa and their native relatives, in addition to being subject to the same predators and pathogens (40, 41). The enemy escape hypothesis also supports this view (42, 43). An alternative, opposing hypothesis is that relatedness to native taxa may convey degrees of preadaptation to the conditions of the invaded environment, rendering close relatives more likely to succeed once introduced (32, 39, 44).Previous studies have been equivocal, finding evidence both for (30, 31, 38, 45–50), and against (24, 32, 41, 44, 51–55) Darwin’s hypothesis. However, few have used a strict phylogenetic approach based on evolutionary divergence, instead predominantly relying on taxonomic ranks (e.g., refs. 45 and 56, reviewed in refs. 57 and 58), which are highly subjective as measures of relatedness (59). In instances where phylogenetic trees were used, some have used supertrees compiled from multiple studies (46, 60, 61), with estimated branch lengths that may not accurately reflect the evolutionary distances between taxa. Other studies have been based on community phylogenetic trees (47, 60, 62). This approach may be problematic, as communities are not necessarily monophyletic groups, but collections of co-occurring species whatever their evolutionary relationships may be (63), and sampling in such studies is unlikely to include adequate representation of all lineages present, whereas phylogenetic analyses assume monophyly of the ingroup and their accuracy is dependent on sampling that is representative of the diversity within (64, 65).This study sought to address theoretical and methodological issues that may have limited progress toward resolving Darwin’s naturalization conundrum (56) by using phylogenies based on molecular markers to assess the evolutionary distances between native and nonnative taxa in a strongly supported monophyletic group, the thistle tribe (Cardueae, Asteraceae), in a well-defined biogeographic area, the California Floristic Province (CAFP) (66, 67). The thistles of California offer an ideal opportunity to test Darwin’s hypothesis. The tribe, which boasts an impressive list of Mediterranean and temperate invaders, is most prolific in Mediterranean climate regions, which not only rank among the most biodiversity-rich biomes on the planet (68, 69), but among the most imperiled as well (70–74). The CAFP is one of such biodiversity hotspots, as defined by Conservation International, and is often recognized as a biogeological entity (75, 76). Also, programs and legislation regarding invasive taxa are usually state specific, making the study of invasive Cardueae in California both politically and biologically meaningful.Phylogenies of Cardueae based on sequences from three genomic regions commonly used in phylogenetic studies of angiosperms were generated with taxon sampling representing the full lineage diversity of the tribe, including all species native and naturalized in the CAFP. Phylogenetic trees were constructed using parsimony, maximum likelihood, and Bayesian approaches. Phylogenetic distances of invasive and noninvasive introduced species from natives were compared using a comprehensive set of metrics and statistical tests to assess the utility of phylogenetic distance from natives as a predictor of invasive behavior. This study finds evidence contrary to Darwin’s hypothesis and demonstrates the robustness of such metrics, which should be more informative and meaningful than taxonomic groupings (30, 46, 77–79), especially when supported by a well-resolved molecular phylogeny.