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Multiple Introductions of Two Invasive Centaurea Taxa Inferred

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Multiple Introductions of Two Invasive Centaurea Taxa Inferred Diversity and Distributions, (Diversity Distrib.) (2008) 14, 252–261 Blackwell Publishing Ltd BIODIVERSITY Multiple introductions of two invasive RESEARCH Centaurea taxa inferred from cpDNA haplotypes Ruth A. Hufbauer1* and René Sforza2 1Department of Bioagricultural Sciences and ABSTRACT Pest Management and Graduate Degree Knowing the origin of invasive taxa, whether multiple introductions have occurred, Program in Ecology, Colorado State University, Fort Collins, CO 80523-1177, USA, 2European and levels of genetic variation relative to the native range, is vital to conducting Biological Control Laboratory, USDA-ARS, rigorous tests of hypotheses to explain biological invasions. We explore phylo- Campus International de Baillarguet, C S90013, geographical relationships of two Eurasian knapweed taxa that are invasive in North Montferrier-sur-Lez, 34988 St-Gely du Fesc, America, Centaurea diffusa and C. stoebe micranthos (Asteraceae), using chloroplast France DNA intron sequences. We also gathered data from C. stoebe stoebe, hybrids between C. diffusa and C. stoebe stoebe (C. xpsammogena), and three other species in the genus. We sequenced 213 individuals from Eurasia and North America, and found 22 haplotypes. Centaurea diffusa has lower haplotype diversity and allelic richness in the introduced range relative to the native range. Even with reduced variation, the data suggest at least two introductions of C. diffusa. There is a trend towards reduced variation in C. stoebe micranthos, but it is not significant. One of the haplotypes found in North American C. stoebe micranthos matches a haplotype from a taxon other than C. stoebe micranthos in Europe. This suggests introgression of the chloroplast between taxa, or possibly the invasion of another Centaurea taxon into North America. Additionally, C. diffusa, C. stoebe micranthos, and C. stoebe stoebe share several haplotypes, including their most common haplotype. This suggests ongoing hybridization between the species or incomplete segregation. These data can guide further exploration for the origins of these species, and point out locations within *Correspondence: Ruth A. Hufbauer, Department of Bioagricultural Sciences and Pest the introduced range with unique and diverse genetic makeup. Management, Colorado State University, 1177 Keywords Campus Mail, Fort Collins, CO 80523-1177, USA. Tel.: 970-491-6945; Fax: 970-491-3862; Exotic plants, biological control, biological invasions, Centaurea maculosa, E-mail: [email protected] haplotype network, invasion, knapweed. genetic surveys. While identifying what taxa have invaded may INTRODUCTION sound simple, often it is not (Jahodová et al., 2007). Even within Biological invasions are crucibles for rapid ecological and the native range, taxa may not be well-defined or described, and evolutionary change: they alter species distributions, ecosystem phenotypic differences between samples from the native and processes, and community structure, and are a key threat to introduced range may make species identification difficult native biodiversity (e.g. Parker et al., 1999; Mack et al., 2000; without the use of molecular markers. Molecular data can Pimentel et al., 2000). Determining the factors that enable an also aid in determining from where in the native range taxa introduced species to proliferate has emerged as a fundamental were introduced, which information is required for rigorous challenge to ecologists and evolutionary biologists worldwide tests of several hypotheses regarding invasion (e.g. the explicitly (Thuiller et al., 2005; Mitchell et al., 2006; PyÍek & Richardson, biogeographical enemy release and EICA hypotheses; Blossey & 2006). Nötzold, 1995; Torchin & Mitchell, 2004). Finally, molecular There are numerous ecological and evolutionary hypotheses genetic data can be used to evaluate how much genetic variation to explain the invasiveness of non-native species (see for example, is present in the introduced range, and how that differs from the Shea & Chesson, 2002; Torchin & Mitchell, 2004; Richardson & native range, which is important in addressing ideas about how PyÍek, 2006; Blank & Sforza, 2007). To test these hypotheses founder effects, hybridization, and outcrossing may inhibit rigorously, we need to know what is present, where it was or facilitate invasions (Ellstrand & Schierenbeck, 2000; Sakai introduced from, and how genetically variable it is, all of which et al., 2001; Kolbe et al., 2004; Facon et al., 2006; Lavergne & can be addressed initially with basic molecular population Molofsky, 2007). In addition to enabling more rigorous tests of DOI: 10.1111/j.1472-4642.2007.00424.x © 2007 The Authors 252 Journal compilation © 2007 Blackwell Publishing Ltd www.blackwellpublishing.com/ddi Phylogeography of two invasive Centaurea taxa ecological and evolutionary hypotheses, an important application et al., 2004). Despite this attention, little is known about the of quantifying genetic variation is to focus work on biological genealogical relationships between individuals from the native control of invasive species. Evaluation of the efficacy of candidate and introduced ranges. Even more importantly, with the agents for biological control should be done on the full range of complexity of the genus, the taxonomic identity of the individuals genotypic diversity present within the introduced range (Gaskin in North America remains uncertain. Positive identification is et al., 2005; Goolsby et al., 2006), thus first that range of diversity complicated by the diversity of taxa within the Centaurea genus must be delineated. in the native range, many of which can be difficult to distinguish The genus Centaurea L. (Asteraceae) has about 300 species morphologically (Ochsmann, 2000). (Garcia-Jacas et al., 2006), many of which have been introduced To move towards rigorous tests of hypotheses to explain and around the world and become invasive. In North America, 34 manage biological invasions, we are exploring the population Centaurea species are reported to be introduced (http:// genetics of the invasion of C. diffusa and C. stoebe micranthos into plants.usda.gov/), 14 of which are defined as noxious weeds in North America. We gathered sequence data from chloroplast one or more states. However, there is uncertainty regarding introns to evaluate the region’s utility and to explore: (1) whether exactly which taxa are present in North America, and their the two species were introduced one or more times into North proper scientific names. This uncertainty is compounded by the America, (2) possible origins in the native range of invasive state of taxonomy of the group: sections within the genus are still individuals, and (3) levels of genetic variation within the native being revised, and relationships within sections are not well and introduced ranges. resolved (Garcia-Jacas et al., 2006). Our research focuses on members of the Centaurea genus METHODS within the section Acrolophus–Phaelolepsis (Garcia-Jacas et al., 2006). Furthermore, we focus on several members of the Plant collections and DNA extractions Centaurea stoebe species group (C. stoebe s.l.), a group of about 33 named taxa (Ochsmann, 2000). Two taxa within C. stoebe s.l., Either fresh leaf tissue or seed were collected from 1 to 30 diffuse and spotted knapweed, have become noxious weeds in individual plants from 30 locations in the native European North America and are the main subjects of this research. Both of range and 20 locations in the introduced North American range these taxa are comprised of diploid (2x = 2n = 18) and tetraploid (Fig. 1, Table 1). Eurasian samples described here were identified (2x = 4n = 36) cytotypes. The cytotypes of diffuse knapweed fall following Turkish and Ukrainian floras, and species assignments under the single scientific name Centaurea diffusa Lam. The were verified by botanists from herbaria in Ukraine (Kiev and nomenclature for spotted knapweed is more complex. The two Yalta), and France (Paris and Montpellier). Leaf tissue was stored cytotypes, which are morphologically indistinguishable, together in silica desiccant until DNA could be extracted. Seeds were come under C. stoebe L, a name that takes precedence over stored in paper coin envelopes, and later germinated in a green- the commonly used C. maculosa (Ochsmann, 2000). The house. At approximately the four-leaf stage, one leaf was harvested monocarpic diploid is designated C. stoebe ssp. stoebe L., and for DNA extraction. Genomic DNA was extracted using the the polycarpic tetraploid is designated C. stoebe ssp. micranthos Dneasy Plant Mini Kit from Qiagen® (Valencia, CA, USA). This (Gugler) Hayek (for which C. biebersteinii DC. is a synonym). study included a total of 213 samples (Table 1). Initially, all plants Diploid C. stoebe stoebe are native to western Europe, and sampled were thought to be C. diffusa, C. stoebe stoebe, C. stoebe tetraploid C. stoebe micranthos are native to eastern Europe and micranthos, C. maculosa albida Lecoq & Lemotte (distinct popula- Asia. The spotted knapweed plants in North America that have tions that may be synonymous with C. stoebe stoebe), C. vallesiaca been surveyed are tetraploids (Müller, 1989; Ochsmann, 2000). D.C. Jord. (a closely related species within the C. stoebe s.l. species Supporting these observations, most plants within North America group from its native Swiss Valais), and C. xpsammogena. are polycarpic (RAH, pers. obs.), and have up to four alleles at Subsequent identification of herbarium specimens, however, microsatellite loci
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