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Hybridization is an important cause of abrupt speciation. Hybrid speciation without a change in ploidy (homoploid hybrid speciation) is well-established in plants but has also been reported in animals and fungi. A notable example of recent homoploid hybrid speciation is Senecio squalidus (Oxford ragwort), which originated in the UK in the 18th Century following introduction of hybrid material from a hybrid zone between S. chrysanthemifolius and S. aethnensis on Mount Etna, Sicily. To investigate genetic divergence between these taxa, we used complementary DNA microarrays to compare patterns of floral gene expression. These analyses revealed major differences in gene expression between the parent species and wild and resynthesized S. squalidus. Comparisons of gene expression between S. aethnensis, S. chrysanthemifolius and natural S. squalidus identified genes potentially involved in local environmental adaptation. The analysis also revealed non-additive patterns of gene expression in the hybrid relative to its progenitors. These expression changes were more dramatic and widespread in resynthesized hybrids than in natural S. squalidus, suggesting that a unique expression pattern may have been fixed during the allopatric divergence of British S. squalidus. We speculate that hybridization-induced gene-expression change may provide an immediate source of novel phenotypic variation upon which selection can act to facilitate homoploid hybrid speciation in plants.

Interspecific hybridization is an important mechanism of speciation in higher plants. In flowering plants, hybrid speciation is usually associated with polyploidy (allopolyploidy), but hybrid speciation without genome duplication (homoploid hybrid speciation) is also possible, although it is more difficult to detect. The combination of divergent genomes within a hybrid can result in profound changes to both genome and transcriptome. Recent transcriptomic studies of wild and resynthesized homoploid and allopolyploid hybrids have revealed widespread changes to gene expression in hybrids relative to expression levels in their parents. Many of these changes to gene expression are 'non-additive', i.e. not simply the sum of the combined expression levels of parental genes. Some gene expression changes are far outside the range of gene expression in either parent, and can therefore be viewed as 'transgressive'. Such profound changes to gene expression may enable new hybrids to survive in novel habitats not accessible to their parent species. Here, we give a brief overview of hybrid speciation in plants, with an emphasis on genomic change, before focusing discussion on findings from recent transcriptomic studies. We then discuss our current work on gene expression change associated with hybrid speciation in the genus Senecio (ragworts and groundsels) focusing on the findings from a reanalysis of gene expression data obtained from recent microarray studies of wild and resynthesized allopolyploid Senecio cambrensis. These data, showing extensive non-additive and transgressive gene expression changes in Senecio hybrids, are discussed in the light of findings from other model systems, and in the context of the potential importance of gene expression change to hybrid speciation in plants.

Allopolyploidy, which involves genome doubling of an interspecific hybrid is an important mechanism of abrupt speciation in flowering plants [1-6]. Recent studies show that allopolyploid formation is accompanied by extensive changes to patterns of parental gene expression ("transcriptome shock") [7-15] and that this is likely the consequence of interspecific hybridization rather than polyploidization [16]. To investigate the relative impacts of hybridization and polyploidization on transcription, we compared floral gene expression in allohexaploid Senecio cambrensis with that in its parent species, S. vulgaris (tetraploid) and S. squalidus (diploid), and their triploid F1 hybrid, S. x baxteri [17]. Major changes to parental gene expression were associated principally with S. x baxteri, suggesting that the polyploidization event responsible for the formation of S. cambrensis had a widespread calming effect on altered gene expression arising from hybridization [17]. To test this hypothesis, we analyzed floral gene expression in resynthesized lines of S. cambrensis and show that, for many genes, the "transcriptome shock" observed in S. x baxteri is calmed ("ameliorated") after genome doubling in the first generation of synthetic S. cambrensis and this altered expression pattern is maintained in subsequent generations. These findings indicate that hybridization and polyploidization have immediate yet distinct effects on large-scale patterns of gene expression.