Origin and diversification of flax and their relationship with heterostyly across the range

Aim: Understanding plant diversity and how different traits have shaped the current biodiversity setting across the world is one of the major challenges for evolutionary biology. In this sense, genus Linum have been broadly studied as a model of species showing heterostyly, but no studies have attempted to investigate possible correlations between heterostyly and diversification. Thus, in this study we aim to explore the origin and diversification of the genus Linum and to determine its centre of diversity and potential source for the colonisation of other areas. Also, we aim to study how heterostyly may have shaped diversification rates and colonisation patterns in the genus. Location: Worldwide (focused on the Western Palearctic). Taxon: Genus Linum L. (Linaceae). Methods: We analysed nuclear ITS and plastid ndhF, matK and trnL-F DNA regions in a total of 103 samples of 93 different species of the genus Linum, as well as seven samples from other Linaceae. We performed divergence time analysis in BEAST2 under a birth-death tree model, then used the resulting tree for an ancestral area reconstruction using the R package “BioGeoBEARS.” Finally, we estimated diversification rates using BAMM and examined the correlation between diversification rates and geographic ranges and heterostyly. Results: Linum s.l. diverged during the late Eocene to mid Oligocene (27.2–38.29 Ma at 95% highest posterior density interval) in the Western Palearctic, where most species diversified. Within-area speciation is the main mechanism of diversification in the genus. Most dispersal events occurred from the Western Palearctic to other regions, probably through long-distance dispersal (LDD). No changes were found regarding diversification rates in specific clades or in relation with reproductive system (heterostyly) or geographic areas. Colonisation of new areas was achieved mostly by monomorphic lineages, whereas heterostylous species mostly remained in the ancestral Western Paleartic area. Main conclusions: The Western Palearctic acted as a source of dispersal in seven out of nine total dispersal events but never as a sink. All species or lineages that colonised new areas after LDD were monomorphic for style length, as predicted by the theory on reproductive traits of colonising species. Thus, heterostyly is shown to affect establishment success in a new area. Neither biogeographic changes nor analysed trait changes can explain speciation nor extinction rates in Linum. Our results confirm that the evolution of heterostyly is related to the paleogeographic history and are not consistent with the idea that a key innovation or “dispersification” has shaped the diversification patterns in Linum.Ministerio de Ciencia e Innovación CGL2013-45037- P, PGC2018-099608- B- 10