Repeated homoploid hybrid speciation (HHS) events with the same parental
species have rarely been reported. In this study, we used population
transcriptome data to test paraphyly and HHS events in one conifer
Picea brachytyla. All analyses identified and supported
non-sister relationships for the two lineages of P. brachytyla.
The southern lineage was placed within the re-circumscribed P.
likiangensis species complex (PLSC) while P. brachytyla sensu
stricto (s.s.), comprising only the northern lineage, parallels both
PLSC and the closely related P. wilsonii. In addition, both
phylogenetic and coalescent analyses suggested that P. brachytyla
s.s. arose from homoploid hybrid speciation between the ancestor of the
PLSC before its diversification (into the current varieties or species),
and P. wilsonii, through an intermediate hybrid lineage at an
early stage and backcrossing to the ancestral PLSC. These two parental
ancestors also produced another homoploid hybrid species, P.
purpurea, in the same way but at a later stage, through the same
extinct lineage but backcrossing to the other parent, P.
wilsonii. We reveal the first case that backcrossing to different
parents of the same extinct hybrid lineage produced two different hybrid
species. Our results highlight the existence of more reticulate
evolution during species diversification in the spruce genus and more
complex homoploid hybrid events than have previously been identified.