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).