INTRODUCTION
Cultivation of plants beyond their native ranges has a long history
(Hobhouse, 1992; Huxley, 1978; Reichard & White, 2001). Although we
often associate this anthropogenic practice with our staple crops,
hundreds of plants are currently cultivated. While cultivation provides
valuable resources to humans, it can have detrimental effects on the
native flora, especially when alien taxa escape their cultivated
lifestyle and re-establish themselves in the wild within or outside
their native ranges (Todesco et al., 2016; Quilodrán et al., 2020b).
Naturalized taxa can for example be highly invasive and outcompete
native species (Anderson, Galatowitsch, & Gomez, 2006; Downey &
Richardson, 2016). In addition, naturalizations can also increase the
opportunities for hybridization and inter-specific gene flow when
previously isolated taxa are brought together (Owen et al., 2020).
Hybridization and gene flow are major drivers of speciation and trait
evolution in plants (Anderson & Stebbins, 1954; Ellstrand &
Schierenbeck, 2000; Morjan & Rieseberg, 2004; Otto & Whitton, 2000;
Rieseberg, 1995; Rieseberg & Burke, 2001; Schierenbeck & Ellstrand,
2009; Soltis et al., 2009; Soltis, Marchant, Van de Peer, & Solitis,
2015; Stebbins, 1959; Yakimowski & Rieseberg, 2014). Gene flow between
divergent lineages can increase genetic diversity and establish novel
stable hybrids that are reproductively isolated from their parental
species, by for example allopolyploidization or clonal propagation, and
thus can evolve into new species (Ainouche et al., 2009; Ellstrand &
Schierenbeck, 2000; Grant, 1981; Mallet, 2007; Morjan & Rieseberg,
2004; Rieseberg & Burke, 2001; Schierenbeck & Ellstrand, 2009; Todesco
et al., 2016; Quilodrán et al., 2020a). However, if the isolating
barriers between hybrids and parental taxa are weak, continued gene flow
between them can result in homogenization and ultimately genetic
swamping with the formation of coalescent complexes (hybrid swarms;
Beninde, Feldmeier, Veith, & Hochkirch, 2018; Ellstrand &
Schierenbeck, 2000; Pinto et al., 2005; Todesco et al., 2016; Quilodrán
et al., 2020a). Hybridization can therefore promote the loss of species
by merging previously separated taxa (Owens & Samuk, 2020; Todesco et
al., 2016; Quilodrán et al., 2020a). Here we explore the genomic and
phenotypic consequences of frequent inter-specific gene flow following
cultivation and naturalization using mints (Mentha ) as our study
system.
Mints are aromatic herbs with cosmopolitan distributions. Several mints
are widely cultivated in many parts of the world for culinary use and
for extraction of essential oils used as flavoring agents (Gobert, Moja,
Colson, & Taberlet, 2002; Singh & Pandey, 2018; Tucker, 2012; Vining
et al., 2020). Although Mentha is a relatively small genus, it is
highly diverse due to inter-fertility between many taxa and numerous
hybrid species are recognized (Gobert et al., 2002; Tucker et al., 1980;
Tucker & Naczi, 2007). Most mint hybrids are sterile but can
successfully propagate clonally using rhizomes (Harley & Brighton,
1977; Gobert et al., 2002). Exceptions to this are hybrids between the
two diploid species M. longifolia (2n=24) and M.
suaveolens (2n=24; Chambers & Hummer, 1994; Harley & Brighton, 1977;
Sobti, 1965). In Europe, where these two taxa are sympatric, they can
spontaneously hybridize forming the partly fertile hybrid complexM. × rotundifolia (Harley & Brighton, 1977). In addition,
the widely cultivated M. spicata (spearmint; Singh & Pandey,
2018; Vining et al., 2020) is often described as an allopolyploid
(2n=48) formed from hybridization of M. longifolia and M.
suaveolens (Chambers & Hummer, 1994; Gobert et al., 2002; Harley &
Brighton, 1977; Sobti, 1965; Tucker et al., 1980; Tucker & Naczi,
2007). However, the allopolyploid status of M. spicata has been
questioned (Heylen, Debortoli, Marescaux, & Olofsson, 2021) and
chromosome counts range between 36 and 72 (Ahmad, Tyagi, Raghuvanshi, &
Bahl, 1992; Chambers & Hummer, 1994; Sobti, 1965). Similarly, there are
reports of polyploid chromosome counts (2n=36/48) for M.
longifolia (Chambers & Hummer, 1994; Harley & Brighton, 1977; Sobti,
1965).
Mentha spicata and its hybrid with M. aquatica , i.e.M. × piperita (peppermint), are the most widely cultivated
mints (Salehi et al., 2018). The exact origin of M. spicata is
unknown, but some studies suggest that it was formed in cultivation
(Harley & Brighton, 1977; Tucker, 2012). Although M. spicata is
considered native to most of continental Europe, the Middle East, and
southern Asia, it has also spread widely from cultivated plants
obscuring its natural range and population size (Gobert et al., 2002;
Harley & Brighton, 1977; Vining et al., 2020). Outside of the
presumably native range, M. spicata is currently naturalized in
most geographic regions with a warm-temperate climate overlapping, and
exceeding, that of the two hypothesized parental taxa (Harley &
Brighton, 1977; Vining et al., 2020). Despite the reported differences
in ploidy, M. spicata frequently forms hybrids with both M.
longifolia and M. suaveolens but the offspring (M. ×villosa-nervata and M. × villosa , respectively) are
believed to be sterile due to their theoretical triploid status
(Chambers & Hummer, 1994; Harley & Brighton, 1977; Gobert et al.,
2002). The re-establishment of cultivated M. spicata in its
native range creates an excellent opportunity to study the phenotypic
and genotypic consequences of increased opportunities for hybridization.
Here we take advantage of the biodiversity stored in herbarium
collections that allows for evaluations of specimens collected over
large geographic regions (Bieker & Martin, 2018). We first evaluate the
morphological spaces of the cultivated M. spicata , the native
species (M. longifolia and M. suaveolens ), and their
hybrids (M. × rotundifolia ). We then use whole genome
sequencing to (1) establish patterns of genetic admixture and gene flow
between taxa, (2) infer the genomic histories of M. xrotundifolia and M. spicata , and (3) test the hypothesis
that increased opportunities for inter-specific gene flow following the
naturalization of the cultivated M. spicata has laid the
foundation for the formation of a coalescent complex.