Introduction

Retracing pathways of species introductions to new lands is a fundamental part of understanding what ecological and evolutionary factors are involved in the successful establishment and spread of species into new ranges (Wilson et al., 2009; Estoup & Guillemaud, 2010; van Kluenen et al., 2015; Seebens et al., 2015; Chapman et al., 2017). The global movement and spread of introduced species have received much attention in recent decades, with particular focus being placed on studying contemporary species invasions that impact socioeconomic well-being and threaten indigenous biodiversity (Mack et al., 2000; Puckett et al., 2016; Chapman et al., 2016; Guo et al., 2017). However, humans have long been mediating the transoceanic dispersal and spread of species both intentionally and accidentally. Retracing pathways of historical invasions is equally important in advancing our understanding of species’ adaptations to new lands and reasons for their success, independent of the ecological or economic effects of such invasions (Mack 2003; Preston, Perlman, & Hall 2004; van Kluenen et al. 2015; Chapman et al. 2017).
The human-mediated dispersal of plants from Europe to other continents became particularly prevalent around the year 1500, a time coinciding with European exploration, the birth of colonialism, and the start of wide-scale changes in human demography, land use, trade and industrial development (Godwin 1944; Pysek, 1988; Preston, Perlman, & Hall, 2004; Mancall 2006; Hulme 2009; Banks et al., 2015; Turbelin et al., 2016). Written accounts from early voyagers and colonists dating back to the 16th and 17th centuries can provide evidence of the introduction of European species to continents such as North America; however, such records are scarce (Fernald, 1900). This, and the poor documentation of native biodiversity prior to arrival of Europeans, hinders our ability to retrace the origins of historical introductions (Estoup & Guillemaud, 2010; Puckett et al., 2020).
Molecular methods have helped to disentangle the origins of a number of introduced plants, by inferring source populations and retracing putative pathways of invasion, and comparing genetic differentiation between native and introduced ranges (Ortiz et al, 2008; Estoup & Guillemaud, 2010; Lambertini et al. 2012; Zhu et al., 2017; Canavan et al. 2017). However, genetic changes within populations over time attributed to admixture or loss of genetic diversity due to founder effects or genetic drift can pose challenges in identifying source populations and inferring dispersal routes for historical introductions (Dluglosch and Parker 2008; Gaskin et al. 2013; Dormontt et al. 2014; Martin et al. 2014;). Advances in genome-wide sequencing technologies now make it possible to genotype individuals using thousands of markers and therefore provide a promising solution to identifying the source of historical introduction events even if genetic differentiation is very low or genetic changes between populations are pronounced (Estoup & Guillmaud, 2010; Elshire et al., 2011; Lu et al., 2013; Vigueira et al., 2013; Narum et al., 2013; Cornille et al., 2016; Puckett et al., 2016).
Here we use the worldwide weed Plantago major L. (Plantaginaceae), also known as common, greater or broadleaf plantain, as a case for understanding human-mediated plant dispersals and potential reasons for successful establishment in new ranges. Native to Europe and Asia, the species grows in a wide range of disturbed habitats (Hawthorn, 1974; Holm et al., 1979; van Dijk, 1984). The species is considered commensal and, based on its medicinal properties, has had a long history of human use in both native and introduced ranges (Samuelsen, 2000; Stepp & Moerman, 2000; Bennett & Prance, 2000; Palmer, 2004). It was introduced to North America by European voyagers or possibly earlier with Norse voyagers (Samuelsen, 2000), and to other parts of the introduced ranges during colonial times, including Australasia, South America, and southern Africa. It is an excellent example of a poorly documented historical plant introduction for which genomic analysis can help unravel. Historical written records and herbarium specimens collected in the introduced ranges before the 19th century are limited and offer limited insights into elucidating the plant’s arrival and early spread outside of its native distribution. Plantago major is known today from every continent except Antarctica (Figure 1 ) and, due to its human-mediated dispersal, is arguably one of the world’s most prevalent weeds (Rousseau, 1966; Holm et al., 1979; van Dijk & Wolff, 1992; Rahn, 1996). By the 17th century, the plant had already been noted to be well-established in New England (northeastern USA), where indigenous peoples referred to the plant as “Englishman’s foot” because it followed colonists wherever they went (Josselyn, 1672). Although the species is considered introduced throughout North America, there are reports suggesting that it, or at least a variety of the species, is native to northern North America, north of 50o latitude, based on the species’ presence in isolated habitats that were considered undisturbed by early Europeans, though this remains unconfirmed (Hawthorn, 1974).
Plantago major has been extensively studied in its native range and a wealth of ecological, physiological and genetic information is available for the species (Mølgaard, 1976; Kuiper & Bos, 1992; Morgan-Richards & Wolff, 1999). It possesses many of the traits that are common amongst the most successful introduced plants (Pysek et al., 2009; Hejda et al., 2014; Pysek et al., 2015), including high phenotypic plasticity, large ecological amplitudes, a high tolerance to human disturbance, rapid growth rates, and the production of propagules with specialized adaptations for long-distance dispersal such as mucilaginous seeds and wind pollination (Young & Evans, 1973; Hawthorn, 1974; van Dijk, 1984; Rahn, 1996; Samuelsen, 2000; Kreitschitz, Kovalev, & Gorb, 2016; Iwanycki Ahlstrand et al, 2018; Iwanycki Ahlstrand et al, 2019). Furthermore, the species is capable of self-fertilizing, meaning that a single propagule can putatively establish sexually reproducing populations in new ranges (Baker, 1974; Wolff, 1991). As with other selfing or clonal species, thousands of individuals of P. majorcan persist in a small area, but low genetic diversity within such populations has been found (van Dijk & van Delden, 1981; Wolff et al., 1994; Wolff & Morgan-Richards, 1998). The low genetic diversity and low heterozygosity associated with highly selfing species suggests that every population of P. major is presumed to be a highly inbred line (Wolff, 1991; Wolff and Morgan-Richards, 1998).
Despite the species being extensively studied in the UK, Denmark and The Netherlands, the genetics of populations elsewhere in its native and introduced ranges have seldom been investigated. The origins and genetic diversity of non-crop plants that have been introduced across the globe, and how genomic variation contributes to the success of global weeds have rarely been studied (but see Ortiz et al, 2008; Cornille et al., 2016; Zhu et al., 2017). To address these gaps, we take a population-genomic approach and analyse thousands of genome-wide single-nucleotide polymorphisms (SNPs), generated by genotyping-by-sequencing (GBS) of Plantago major sampled from 50 populations across its global range to (1) infer ancestral origins of introduced populations, and (2) retrace pathways of introduction to new ranges including North and South America, Greenland, Iceland, Africa, Hawaiʻi, the Canary Islands, Australia and New Zealand. GBS was chosen based on its application to population genomics in non-model plants (Lu et al., 2013). We test the hypotheses that P. major was dispersed by Europeans during colonial times and that a high level of genetic differentiation was not necessary for the successful establishment and spread of introduced plants. This knowledge can help us understand the dispersal and establishment of new potential plant introductions as well as how introduced plants cope under climate change.