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.