Factors affecting cross-ploidy hybridisation and introgression
Cross-ploidy hybrids can arise in a variety of situations. Many, but not all, examples occur in contact zones between parental species with contrasting ploidy, where hybrid zones and hybrid swarms may form. Some of these hybrid zones have shifted over time (e.g. Betula , Wang et al., 2014), or are mosaic in structure (Popelka et al., 2019). In addition, there are notable differences in genetic structure between contact zones, with some comprising a swarm of F1, F2 and backcrossed hybrids (Fearn, 1977), indicative of low genetic divergence between parental species (Edmands, 2002), while others contain only a few early generation hybrids, suggesting that parental species are more distantly related, and show higher levels of reproductive isolation (Koutecky et al., 2011). Hybrids may also occur in the absence of one or both parents, normally where greater lifespans allow persistence long after hybrid formation (Bailey, 2013; Preston & Pearman, 2015). Where cross-ploidy hybrids are present without their parents, they may represent stable lineages that survive through asexual reproduction (e.g. vegetative reproduction or apomixis), and are therefore different to some ephemeral forms present in hybrid zones.
The direction of introgression in cross-ploidy hybrids is overwhelmingly towards the higher ploidy parent (Table 1). This is unsurprising as the union of an unreduced 2n = 2x gamete of a diploid and a reduced n = 2x gamete of a tetraploid provides a direct pathway for introgression in this direction, whereas the alternative direction is a two-step process via the triploid bridge (Baduel et al., 2018; Stebbins, 1971). As such, only two plant studies and one animal study report the opposite scenario (Aconitum and Euphrasia ,Neobatrachus ; Sutkowska et al., 2017; Yeo, 1956), and a further three studies report bidirectional introgression (in Betula, Rorippa , and Chrysanthemum , Bleeker, 2003; Qi et al., 2022; Thorsson et al., 2007). However, other factors may still pose limits for introgression in the direction of the higher ploidy parent. Polyploids evolve meiotic stability to ensure reliable segregation of additional chromosomes at meiosis, with loci underlying tetraploid meiotic stability shown to be under selection in natural populations of autotetraploid Arabidopsis arenosa (Hollister et al., 2012). Cytogenetic evidence in Arabidopsis suggests introgression from diploids to tetraploids may introduce genetic variants that disrupt regular meiosis in tetraploids (Morgan et al., 2020).
A key determinant of the outcomes of cross-ploidy hybridisation is the ploidy of the parents, and the mode of ploidy (whether the parents are auto or allopolyploids). In terms of ploidy, it is clear that successful cross-ploidy hybridisation may occur more frequently between cytotypes of higher ploidy (e.g. tetraploids and hexaploids) than of lower ploidy (e.g. diploids and tetraploids, Hülber et al., 2015; Sutherland et al., 2020). However, despite the apparent weakening of postzygotic barriers at higher ploidy levels, prezygotic barriers may be strong enough for such cross-ploidy hybridization to remain relatively rare (Hülber et al., 2015). In terms of mode of ploidy, in allotetraploid parents characterised by disomic inheritance, preferential chromosome pairing between the most similar, homeologous subgenomes, may lead to a subset of polyploid variation introgressing. In contrast, in autotetraploids with tetrasomic inheritance, free recombination between chromosomes may allow any region of the tetraploid to introgress. According to our literature survey, in 21 of 25 studies for which relevant information is available the higher ploidy parent was an allopolyploid. While allopolyploids garner more research interest than autopolyploids in studies of hybridisation (Spoelhof et al., 2017), the higher number of studies reporting allopolyploids may be biologically significant. For example, chromosome pairing of an allotetraploid subgenome more related to the diploid parent could lead to higher probabilities of successful hybridisation than in diploid-autotetraploid hybridisation, where chromosome pairing is disrupted.