Being in the right place at the right time? Parallel diversification bursts favored by the persistence of ancient epizoochorous traits and hidden factors in Cynoglossoideae

PREMISE OF THE STUDY: Long-distance dispersal (LDD) syndromes, especially endozoochory, facilitate plant colonization of new territories that trigger diversification. However, few studies have analyzed how epizoochorous fruits influence both range distribution and diversification rates. We examined the evolutionary history of a hyperdiverse clade of Boraginaceae (subfamily Cynoglossoideae, eight tribes, ~60 genera, ~1100 species) and the evolution of fruit traits. We evaluated the evolutionary history of diaspore syndromes correlated with geographic distribution and diversification rates over time. METHODS: Plastid DNA regions and morphological traits associated with dispersal syndromes were analyzed for 71 genera (226 species). We employed trait-dependent diversification analysis (HiSSE) and biogeographic reconstruction (Lagrange) using a time-calibrated phylogeny. KEY RESULTS: Our results indicate that (1) the earliest divergence events in Cynoglossoideae occurred in the central-northeastern Palearctic during the Paleogene (early to middle Eocene); (2) an epizoochorous trait (specialized hooks named glochids) is ancestral and has been maintained long term; and (3) glochids are correlated with increased diversification rates in two distantly related clades (Rochelieae and Cynoglossinae). Rapid speciation occurred for these two groups in the same area (central-eastern Palearctic) and same period (Oligocene-Miocene: Rochelieae, 30.82-13.69 mya; Cynoglossinae, 33.10-15.21 mya). Lower diversification rates were inferred for the remaining four glochid-bearing clades. CONCLUSIONS: One more example of "biogeographic congruence" in angiosperms is supported by a shared geographic (central-northeastern Palearctic) and temporal (28.60-21.59 mya, late Oligocene) opportunity window for two main clades' diversification. Epizoochorous traits (fruit glochids) had an effect in higher diversification rates only with the joint effect of other unmeasured factors.