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.