Hybrid speciation in angiosperms: parental divergence drives ploidy

Abstract

Hybridization and polyploidy are now hypothesized to have regularly stimulated speciation in angiosperms, but individual or combined involvement of these two processes seems to involve significant differences in pathways of formation, establishment and evolutionary consequences of resulting lineages. We evaluate here the classical cytological hypothesis that ploidy in hybrid speciation is governed by the extent of chromosomal rearrangements among parental species. Within a phylogenetic framework, we calculate genetic divergence indices for 50 parental species pairs and use these indices as surrogates for the overall degree of genomic divergence (that is, as proxy for assessments of dissimilarity of the parental chromosomes). The results confirm that genomic differentiation between progenitor taxa influences the likelihood of diploid (homoploid) versus polyploid hybrid speciation because genetic divergence between parents of polyploids is found to be significantly greater than in the case of homoploid hybrid species. We argue that this asymmetric relationship may be reinforced immediately after hybrid formation, during stabilization and establishment. Underlying mechanisms potentially producing this pattern are discussed.

Fig. 1

Box plots of the distribution of genetic divergence index (GDI) of parental pairs for homoploid and polyploid hybrids. The two groups have an asymmetric dispersion range, with the parents of allopolyploids being more divergent than those producing diploid hybrid species (Mann-Whitney U test, P < 0.0001, see text). The difference in sample sizes probably reflects the greater difficulty of identifying homoploid hybrids.

Fig. 2

(a). Histogram illustrating the different frequency distribution of parental GDI classes for homoploid hybrid species (grey bars) and allopolyploids (open bars). Values on the x-axis show the limits of the GDI classes, with a 0.25 increment. (b). Hypothetical relationships between frequency of occurrence and degree of genomic divergence of parental pairs for allopolyploids (goodness-of-fit to the data R² = 0.815) and homoploid hybrids (goodness-of-fit R² = 0.804), derived from A. There is an equal probability of hybrid formation with and without a change of ploidy when Pd is three quarters of Av (GDI ≈ 0.75). Pd - parental genetic distance; Av - average genetic distance in the genus being studied.