Patterns of genomic variation reveal a single evolutionary origin of the wild allotetraploidMimulus sookensis

Abstract

Polyploidy occurs across the tree of life and is especially common in plants. Because newly formed cytotypes are often incompatible with their progenitors, polyploidy is also said to trigger ″instantaneous″ speciation. If a polyploid can self-fertilize or reproduce asexually, it is even possible for one individual to produce an entirely new lineage, but how often this scenario occurs is unclear. Here, we investigate the evolutionary history of the wild allotetraploidMimulus sookensis, which was formed through hybridization between self-compatible, diploid species in theMimulus guttatuscomplex. We generate a chromosome-scale reference assembly forM. sookensisand define its distinct subgenomes. Despite previous reports suggesting multiple origins of this highly selfing polyploid, we discover patterns of population genomic variation that provide unambiguous support for a single origin, which occurred ~71,000 years ago. OneM. sookensissubgenome is clearly derived from the selferM. nasutus, which organellar variation suggests is the maternal progenitor. The ancestor of the other subgenome is less certain, but it shares variation with bothM. decorusandM. guttatus, two outcrossing diploids that overlap broadly withM. sookensis. This study establishesM. sookensisas an example of instantaneous speciation, likely facilitated by the polyploid′s predisposition to self-fertilize.