The early stages of polyploidy: Rapid and repeated evolution in Tragopogon

Abstract

Elucidating the causes and consequences of polyploidy (whole-genome duplication; WGD) is arguably central to understanding the evolution of most eukaryotic lineages. However, much of what we know about these processes is derived from the study of crops and synthetic polyploids. Tragopogon provides the unique opportunity to investigate the genetic and genomic changes that occur across an evolutionary series from F1 hybrids, synthetic allopolyploids, independently formed natural populations of T. mirus and T. miscellus that are 60-80 years post-formation, to older Eurasian polyploids that are dated by molecular clocks at several million years old, and finally to a putative ancient polyploidization thought to have occurred prior to or early in the history of the Asteraceae (40-43 mya). Tragopogon joins other well-studied natural polyploid systems (e.g., Glycine, Nicotiana, Gossypium, Spartina, Senecio), but presents a range of research possibilities that is not available in any other system. We have shown in T. mirus and T. miscellus that upon allopolyploidization, massive gene loss occurs in patterns that are repeated across populations of independent origin and with a bias against genes derived from T. dubius, the diploid parent shared by both new allotetraploids. We have also shown significant changes in gene expression (transcriptomic shock) in the early generations of allopolyploidy in these species. Massive and repeated patterns of chromosomal variation (intergenomic translocations and aneuploidy) have been revealed by fluorescence in situ hybridization. Aneuploidy results in substitutions between homeologous chromosomes, through reciprocal monosomy-trisomy (1:3 copies) or nullisomy-tetrasomy (0:4 copies). We propose that substantial chromosomal instability results in karyotype restructuring, a likely common process following WGD and a driver of allopolyploid speciation, which has largely unexplored implications for gene losses, gains, and expression patterns. But gene loss and expression changes as well as karyotypic changes are ongoing in T. mirus and T. miscellus, in that no population is fixed for any of these events; thus, we have literally caught evolution in the act.