Hybridization and speciation.

Hybridization has many and varied impacts on the process of speciation. Hybridization may slow or reverse differentiation by allowing gene flow and recombination. It may accelerate speciation via adaptive introgression or cause near-instantaneous speciation by allopolyploidization. It may have multiple effects at different stages and in different spatial contexts within a single speciation event. We offer a perspective on the context and evolutionary significance of hybridization during speciation, highlighting issues of current interest and debate. In secondary contact zones, it is uncertain if barriers to gene flow will be strengthened or broken down due to recombination and gene flow. Theory and empirical evidence suggest the latter is more likely, except within and around strongly selected genomic regions. Hybridization may contribute to speciation through the formation of new hybrid taxa, whereas introgression of a few loci may promote adaptive divergence and so facilitate speciation. Gene regulatory networks, epigenetic effects and the evolution of selfish genetic material in the genome suggest that the Dobzhansky-Muller model of hybrid incompatibilities requires a broader interpretation. Finally, although the incidence of reinforcement remains uncertain, this and other interactions in areas of sympatry may have knock-on effects on speciation both within and outside regions of hybridization.

On the origins of species: does evolution repeat itself in polyploid populations of independent origin?

Multiple origins of the same polyploid species pose the question: Does evolution repeat itself in these independently formed lineages? Tragopogon is a unique evolutionary model for the study of recent and recurrent allopolyploidy. The allotetraploids T. mirus (T. dubius x T. porrifolius) and T. miscellus (T. dubius x T. pratensis) formed repeatedly following the introduction of three diploids to the United States. Concerted evolution has consistently occurred in the same direction (resulting in loss of T. dubius rDNA copies). Both allotetraploids exhibit homeolog loss, with the same genes consistently showing loss, and homeologs of T. dubius preferentially lost in both allotetraploids. We have also documented repeated patterns of tissue-specific silencing in multiple populations of T. miscellus. Hence, some aspects of genome evolution may be "hardwired," although the general pattern of loss is stochastic within any given population. On the basis of the study of F(1) hybrids and synthetics, duplicate gene loss and silencing do not occur immediately following hybridization or polyploidization, but gradually and haphazardly. Genomic approaches permit analysis of hundreds of loci to assess the frequency of homeolog loss and changes in gene expression. This methodology is particularly promising for groups such as Tragopogon for which limited genetic and genomic resources are available.

Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids.

Whole-genome duplication (polyploidisation) is a widespread mechanism of speciation in plants. Over time, polyploid genomes tend towards a more diploid-like state, through downsizing and loss of duplicated genes (homoeologues), but relatively little is known about the timing of gene loss during polyploid formation and stabilisation. Several studies have also shown gene transcription to be affected by polyploidisation. Here, we examine patterns of gene loss in 10 sets of homoeologues in five natural populations of the allotetraploid Tragopogon miscellus that arose within the past 80 years following independent whole-genome duplication events. We also examine 44 first-generation synthetic allopolyploids of the same species. No cases of homoeologue loss arose in the first allopolyploid generation, but after 80 years, 1.6% of homoeologues were lost in natural populations. For seven homoeologue sets we also examined transcription, finding that 3.4% of retained homoeologues had been silenced in the natural populations, but none in the synthetic plants. The homoeologue losses and silencing events found were not fixed within natural populations and did not form a predictable pattern among populations. We therefore show haphazard loss and silencing of homoeologues, occurring within decades of polyploid formation in T. miscellus, but not in the initial generation.

Empirical study of hybrid zone movement.

Hybrid zones are 'natural laboratories' for studying the origin, maintenance and demise of species. Theory predicts that hybrid zones can move in space and time, with significant consequences for both evolutionary and conservation biology, though such movement is often perceived as rare. Here, a review of empirical studies of moving hybrid zones in animals and plants shows 23 examples with observational evidence for movement, and a further 16 where patterns of introgression in molecular markers could be interpreted as signatures of movement. The strengths and weaknesses of methods used for detecting hybrid zone movement are discussed, including long-term replicated sampling, historical surveys, museum/herbarium collections, patterns of relictual populations and introgression of genetic markers into an advancing taxon. Factors governing hybrid zone movement are assessed in the light of the empirical studies, including environmental selection, competition, asymmetric hybridization, dominance drive, hybrid fitness, human activity and climate change. Hybrid zone movement means that untested assumptions of stability in evolutionary studies on hybrid zone can lead to mistaken conclusions. Movement also means that conservation effort aimed at protecting against introgression could unwittingly favour an invading taxon. Moving hybrid zones are of wide interest as examples of evolution in action and possible indicators of environmental change. More long-term experimental studies are needed that incorporate reciprocal transplants, hybridization experiments and surveys of molecular markers and population densities on a range of scales.