Introduction
Climate change, habitat disturbance, and large-scale translocations
resulting from human activities are increasing contacts between species
previously isolated by geographical and ecological barriers, thus
raising their potential to hybridise (Brennan et al., 2014; Crispo et
al, 2011; Larson et al., 2019). Closely related species isolated only by
prezygotic barriers are more likely to hybridise (Vallejo-Marin &
Hiscock, 2016), but even species isolated by very strong postzygotic
barriers do hybridise in some instances. Polyploidy (whole genome
duplication), which is particularly common in plants, creates a very
strong postzygotic barrier between species. Cross-ploidy hybridisation
is therefore usually considered rare because hybrids will have
unbalanced chromosome content and therefore irregular pairing of
chromosomes, rendering the hybrid infertile (Ramsey & Schemske, 1998).
Should a triploid hybrid form, it is normally either completely or
partially sterile, due to the formation of malfunctioning gametes
containing unbalanced chromosome numbers. On occasion, however, some
species differing in ploidy do produce hybrid offspring. The importance
of such events is not to be underestimated; for example, cross-ploidy
hybridisation has led to some very recently originated plant species,
which are now models for the study of polyploid speciation
(Vallejo-Marin & Hiscock, 2016), and also to the origin of some of our
most important crop plants, including wheat, sweet potato, sugar cane
and oilseed rape (Matsuoka, 2011; Yang et al., 2017; Wang et al., 2023;
Zhang et al., 2018). Nonetheless, the frequency of cross-ploidy (or
interploidy) hybridisation in the wild is a neglected topic, with
information scattered through the literature. Here, we bring this
information together and consider its biological significance.
The first known artificial hybrid from crossing two parents of differing
ploidy level was created by Kölreuter in 1761 between diploidNicotiana paniculata and allotetraploid N. rustica.This hybrid was known as the first “botanical mule” due to its
shrivelled anthers and malformed ovaries, indicative of sterility
(Roberts, 1929). Further artificial crosses demonstrated the formation
of other cross-ploidy hybrids that were partially or completely sterile,
but nothing was discovered of the frequency or importance of the
phenomenon in the wild until much later (Lawrence, 1936). Beginning
around the mid-twentieth century, cytogenetic studies became more
frequent and revealed extensive ploidy variation both within and between
species, and which could be used to explain evolutionary relationships
(Love & Love, 1943; Stebbins, 1956). However, it was with the
availability of multiple nuclear markers in the 1990s that researchers
reliably detected hybridisation and introgression between species of
differing ploidy (Abbott et al., 1992; Nason et al., 1992). Now, by
examining many thousands of genetic markers or the complete genomes of
target species, there is potential to detect cases of adaptive
introgression (Suarez-Gonzalez et al., 2018). Moreover, through focusing
on specific genes, examples are now known of cross-ploidy introgression
resulting in the transfer of particular traits that markedly affect the
biology and fitness of recipient species (Baduel et al., 2018; Chapman
& Abbott, 2010; Kim et al., 2008; Monnahan et al., 2019)
While there have been many recent reviews on evolutionary mechanisms the
prevalence of polyploids in nature (e.g. Alix et al., 2017; Chen, 2010;
Kohler et al., 2010; Marques et al., 2018; Soltis et al., 2004), and on
the importance of natural hybridisation (Abbott et al., 2013; Moran et
al., 2021; Soltis & Soltis, 2009; Suarez-Gonzalez et al., 2018; Taylor
& Larson, 2019; Todesco et al., 2016), our aim is to reconcile early
work on cytological variation with recent work on genomics, to consider
whether cross-ploidy hybridisation may be more prevalent and important
than previously known. We first summarise the ways in which cross-ploidy
hybrids may form. Next, we review the prevalence of cross-ploidy
hybridisation, both in the case of the British and Irish flora, which
includes comprehensive data on hybridisation and ploidy, and in the
wider published literature, allowing us to generalise about the
occurrence in nature. Lastly, we explore the biology of cross-ploidy
hybrids and the potential long-term evolutionary outcomes, and discuss
how advances in sequencing technologies and analytical tools may aid
detection to assess more accurately the state of cross-ploidy
hybridisation in nature. We emphasise case studies in flowering plants,
where hybridisation and polyploidy are particularly prevalent and
well-documented, but also consider other organismal groups where
cross-ploidy hybridisation may occur.