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.