Frequency and occurrence of natural cross-ploidy hybrids
Of major interest is how common cross-ploidy hybrids are in nature given the varied constraints of both pre and postzygotic isolation in their generation. In cross-ploidy hybridisation the usual reproductive barriers to cross species mating apply, such as differences in geography, phenology, morphology and mating system (Kay, 2006; Laport et al., 2016; Martin & Willis, 2007), along with specific factors associated with ploidy level difference between parental species, such as the sterility barriers outlined above. The evidence required to prove cross-ploidy hybridisation is confirmation of parental ploidy differences, which may come from chromosome counts (Rice et al., 2015), genome size estimates (Leitch, 2019) or genomic information (Ranallo-Benavidez et al., 2020), and evidence of hybridisation, which may be from genetic data or from other sources such as morphology (Rieseberg & Ellstrand, 1993; though see issues with using morphological data to detect hybrids, below).
There are increasingly comprehensive surveys of ploidy variation that provide key contextual information as to where cross ploidy hybrids could occur and set an upper boundary in term of their number. Worldwide, the majority of plant species are diploid (Rice et al., 2019), however extensive variability in ploidy levels exist at all taxonomic levels and scales (Kolar et al., 2017; Soltis et al., 2010). For example, the genus Sedum in the Crassulaceae ranges from diploid to 80-ploid, which is currently the highest known amongst flowering plants (Bennett & Leitch, 1997). Many commonly studied species also exhibit ploidy variation such as Senecio carolinensis (diploid to 9-ploid; Kolář et al., 2017), and this variation has even been correlated with latitudinal gradients (Zhang et al., 2019). Climatic effects, which include latitude, along with clade specific effects are known to have a role in unreduced gamete formation, a key factor in polyploid genesis (Bretagnolle & Thompson, 1995; Kreiner et al., 2017a, Rice et al., 2019). In contrast to flowering plants, polyploidy in animals and fungi is thought to be rare, famously so in mammals and birds, though many examples are known in certain lineages of amphibians, teleost fish and reptiles (Spoelhof et al., 2020).
While there are extensive estimates of ploidy variation across the Tree of Life, the frequency of cross-ploidy hybridisation remains unknown. Our best general estimate of this in plants may come from the British and Irish flora, which contains a manageable number of native species (~1500, excluding large taxonomically complex groups, Stace, 2019), and is exceptional in having near complete information on species chromosome counts (Henniges et al., 2022), and the extent of natural hybridity (Stace et al., 2015). This extensive dataset has previously been used to estimate that 25% of plant species in the flora hybridise (Mallet, 2005), providing a general estimate for the frequency of hybridisation across diverse plant genera. More recently, a study employing phylogenetic mixed models showed that species that differ in ploidy are 35% less likely to form a hybrid (Brown et al., 2023), though there are still numerous cross-ploidy hybrids, which highlights that ploidy level is far from an absolute barrier to hybridisation.
To further quantify the potential for cross-ploidy hybridisation, we revaluated the available data for the British flora. Ploidy level inferred from available genome size and chromosome counts for flowering plant species (n = 1295 species with data, Brown et al., 2023), shows most species are diploids (56%), with higher ploidy levels becoming exponentially less common (Figure 3). However, there is notable variation when ploidy level is evaluated across the phylogeny for the British flora, with some families showing much more ploidy variation than others, altering the raw material for cross-ploidy hybridisation to act on (Supplementary Figure 1). In terms of the frequency of cross-ploidy hybrids, we analysed hybrids and their parentage identified in the ‘Hybrid Flora of the British Isles’ (Stace et al., 2015), coupled with ploidy level estimates (Brown et al., 2023), to quantify their occurrence. Of the 588 hybrids that have ploidy information for both parents (321 hybrids lack appropriate data), 203 cross-ploidy hybrids have formed (35%; Supplementary Table 1), in comparison to 385 intraploidy hybrids (65%). Cross-ploidy hybrids occur in 67 genera, with over a quarter present in Rumex (Polygonaceae, 24),Salix (Salicaceae, 19) and Euphrasia (Orobanchaceae, 13; Figure 4). The majority (55%) of cross-ploidy hybrids involve diploid-tetraploid crosses, with higher order ploidy crosses closely following (43%), and diploid-triploid crosses in the minority (2%). These results show that cross-ploidy hybrids are relatively common in the British flora, and are present in many different plant groups but overrepresented in few.