Increased opportunities for hybridization can merge species into a coalescent complex
Inter-fertility of the taxa in Mentha subgen. Mentha is well known and species barriers are possibly retained by the formation of sterile hybrids and/or usage of distinct ecological niches (Harley & Brighton, 1977; Gobert et al., 2002). However, the emergence of the fertile allopolyploid M. spicata followed by its re-establishment following cultivation in the native range of M. longifolia andM. suaveolens has resulted in frequent gene flow between the classically recognized taxa (Figure 2; Harley & Brighton, 1977). Indeed, all morphologically and genomically defined groups of specimens show very low levels of genetic distances not consistent with divergent species (Table 2; Meirmans & Hedrick, 2011; Roux et al., 2016). In particular, the genomic differentiation between M. longifolia andM. spicata is elusive (Figure 2 and Table 2). The extensive genetic admixture points to a breakdown of reproductive barriers between taxonomic units and morphological groups. However, given the frequent hybridization of M. longifolia and M. suaveolens in areas of sympatry (Harley & Brighton, 1977) it is unlikely that these taxa have ever been completely reproductively isolated. The emergence of the allopolyploid M. spicata has further promoted the introgression between M. longifolia and M. suaveolens by acting as a genomic bridge (McDonald, Parchman, Bower, Hubert, & Rahel, 2008; Sigel, 2016). The preferential crossing of M. spicata to M. longifolia has resulted in low levels of genetic differentiation between them (Table 2) and has transferred M. suaveolens genes into a mostly M. longifolia genomic background (Figure 2). Overall, our genomic analyses point to genetic swamping and an on-going merging of M. longifolia , M. suaveolens , M. spicata , and their hybrids into a coalescent complex (Beninde et al., 2018; Ellstrand & Schierenbeck, 2000; Pinto et al., 2005; Todesco et al., 2016; Quilodrán et al., 2020a). However, we do find that someF ST-outlier scaffolds contain genes with a function in reproduction, and in particular, pollen recognition (Table S4), which do suggest that there might be some genetic barriers to cross-fertilization between the analyzed mint species, especially between the native mints.
Human assisted movements of species, including cultivation and rearing of species outside their native ranges have undoubtedly changed many ecosystems. On the one hand the addition of species to new ranges increases biodiversity by adding to the total number of species recorded in any one location (Schlaepfer, Sax, & Olden, 2011; Hallman, Olsson, & Tyler, 2022). However, although increased biodiversity is often regarded as positive, shifts in ecosystem compositions can have detrimental effects in the long term. For example, biodiversity might drastically decrease due to alien taxa out-competing native species (Pyšek et al., 2012). In addition, hybridization between native and introduced taxa can also change the local biodiversity (Wolf, Takebayashi, & Rieseberg, 2001). The exact effect of hybridization on local biodiversity is largely controlled by the strength of reproductive barriers between hybrids and parents and here we show that when the reproductive barriers are weak genetic swamping is a likely outcome (Lowry, 2008). Climate changes associated with anthropogenic activities will cause shifts in geographic ranges and ecological niches (Kelly & Goulden, 2008; Chen, Hill, Ohlemüller, & Thomas, 2011) and similar to naturalizations of cultivated taxa this will bring previously isolated taxa into contact with each other and increase the opportunities for hybridization and inter-specific gene flow. As we show here this can indeed promote gene flow between species and speed up the formation of new coalescent complexes.