Evolutionary outcomes of cross-ploidy hybridisation
Recent cross-ploidy hybridisation has led to notable examples of
speciation (<200 years). This has occurred in the plant generaSenecio (Abbott & Lowe, 2004; Lowe & Abbott, 2004) andMimulus (Vallejo-Marin, 2012). These hybrids are also notable in
the context of the British Isles, as they involve alien species as
either one, or both parental species. Similarly, in Rosa one of
the parents, while in Fallopia both parents, involved in
cross-ploidy hybridisation are alien species (Table 1). Human mediated
translocations of species clearly have a profound effect on cross-ploidy
hybridisation. Older hybrid species (10,000+ years) have also originated
in a similar way to Senecio and Mimulus hybrid species,
with this inferred either through morphology and cytogenetic analysis,
or through sequence analysis showing ‘ghost’ subgenomes of allopolyploid
species (e.g. Euphrasia and Packera, Kowal et al., 2011;
Yeo, 1956).
For a hybrid lineage to persist, reproductive isolation between the
newly formed hybrid and the parental progenitors is paramount. Unlike
cases of polyploid hybrid speciation where the hybrid is of differing
ploidy level to both parents, backcrossed F1 hybrids derived from
cross-ploidy hybridisation will match one parental ploidy and therefore
lack the strong reproductive barrier that polyploidy confers. In this
case, other factors must contribute to reproductive isolation, including
ecological selection, niche differentiation, selfing, and chromosomomal
or genetic sterility barriers (Grant, 1981; Gross & Rieseberg, 2005;
Lowe & Abbott, 2004; Rieseberg, 1997). Lastly, reproductive isolation
of a cross-ploidy hybrid can occur by the doubling of the triploid F1
chromosome complement to produce a fertile hexaploid that is isolated by
ploidy level from the parental species, as with Senecio
cambrensis (Abbott and Lowe, 2004) and Mimulus peregrinus(Vallejo-Marin, 2012).
In addition to cross-ploidy hybridisation between species, much early
work, both theoretical and empirical, has explored crosses within
mixed-ploidy species complexes (Fowler & Levin, 1984; Levin, 1975;
Lumaret & Barrientos, 1990). The outcomes of crosses within (diploid x
autopolyploid) or between species (diploid x
autopolyploid/allopolyploid) are similar in many cases; with triploid
hybrids still formed (De Hert et al., 2012; Vandijk et al., 1992),
unreduced gametes remaining an important driver of hybridisation (Baduel
et al., 2018; Lihova et al., 2004), and the direction of introgression
usually being towards the higher ploidy parent (Table 1; Pinheiro et
al., 2010; Stebbins, 1956). On the other hand, between species
hybridisation can lead to higher levels of genetic variation through
fixed heterozygosity in hybrids, and backcrossing to parental species,
resulting in higher fitness (Ramsey & Schemske, 2002). In addition, the
higher the divergence between species, the higher the likelihood of
whole genome duplication post hybridisation, and therefore the
generation of novel polyploid species (Paun et al., 2009).
More than 60 years ago, Stebbins (1956) proposed that within polyploid
complexes a widespread tetraploid could acquire genes via unilateral
introgression from ecogeographicaly isolated diploid taxa occurring
sympatrically with it in different parts of its range. In this way,
several different forms of a tetraploid might originate, with each one
bearing a close resemblance to the local diploid it hybridised with.
Based on cytotaxonomic evidence, Stebbins (1956, 1971) suggested this
has occurred in numerous polyploid complexes of a number of plant
genera, including Dactylis , Knautia , Grindelia ,Phacelia and Campanula . Recently, genomic evidence has
been obtained to provide support for Stebbins’ proposal from work
conducted on a polyploid complex comprising diploid and tetraploid forms
of Arabidopsis arenosa in Europe (Arnold et al., 2015). Genomic
analysis indicates that autotetraploid A. arenosa arose once
before splitting into five major lineages as it spread into different
parts of Central Europe (Arnold et al., 2015). For two of the lineages,
there is evidence that particular haplotypes, not found in any other
tetraploid lineage, are shared with proximal diploid forms of A.
arenosa , indicating these haplotypes were acquired from the local
diploid type and are adaptive (Arnold et al., 2015). In addition, one of
the five tetraploid lineages is a ruderal form, widely distributed along
the railways of Central and Northern Europe. Subsequent analysis
indicates that the widespread lowland form of this early flowering and
rapid cycling “railroad ecotype” likely originated as a result of
introgression of genes from diploid A. arenosa occurring on the
Baltic Coast of Germany and Poland into local populations of the
tetraploid (Baduel et al. 2018a; Monnahan et al. 2019).