Present-day sympatry belies the evolutionary origin of a high-order polyploid.

Summary Disentangling the evolutionary histories of polyploids, especially those with high ploidies, can reveal fundamental processes in speciation. Despite occurring frequently during evolution, the origins of many extant polyploid plant species remain largely unknown. By integrating linkage mapping, polyploid phylogeny and sex-determining region (SDR) in a unified framework, we statistically evaluated evolutionary hypotheses concerning the origin of a recently recognized decaploid strawberry (Fragaria cascadensis). The maximum-likelihood phylogenies and topology tests across homeologous groups consistently rejected the seemingly parsimonious hypothesis of ‘contemporary sympatric speciation’ via hybridization between octoploid and diploid congeners. Instead, most chromosomes supported ‘ancient hybrid speciation’ between a maternal octoploid progenitor ancestral to extant octoploid strawberries and a paternal, extinct Fragaria iinumae-like diploid progenitor, probably in Beringia during the Pleistocene. The absence of a shared SDR between the decaploid and other Fragaria is also consistent with an older origin rather than a recent hybrid origin in situ. Our study reveals a long evolutionary history of the decaploid despite its recent discovery, and highlights the pitfalls of inferring polyploid origins from niche/range alone or combined with morphology. It can serve as an exemplary starting step towards building much-needed model systems of established polyploids that have been, and remain to be, recognized.