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.