Style polymorphism in Linum (Linaceae): a case of Mediterranean parallel evolution?

Abstract

•Heterostyly is a sex polymorphism that has challenged evolutionary biologists eversince Darwin. One of the lineages where heterostyly and related stylar conditionsappear more frequently isLinum(Linaceae). This group is particularly suitable fortesting competing hypotheses about ancestral and transitional stages on the evolution-ary building up of heterostyly.•We generated a phylogeny ofLinumbased on extensive sampling and plastid andnuclear DNA sequences, and used it to trace the evolution of character states of stylepolymorphism. We also revised available data on pollination, breeding systems, andpolyploidy to analyse their associations.•Our results supported former phylogenetic hypotheses: the paraphyly ofLinumandthe non-monophyly of current taxonomic sections. Heterostyly was common in thegenus, but appeared concentrated in the Mediterranean Basin and the South AfricanCape. Ancestral character state reconstruction failed to determine a unique state as themost probable condition for style polymorphism in the genus. In contrast, approachherkogamy was resolved as ancestral state in some clades, giving support to recenthypotheses. Some traits putatively related to heterostyly, such as life history and poly-ploidy, did show marginal or non-significant phylogenetic correlation, respectively.Although pollinator data are limited, we suggest that beeflies are associated with speci-fic cases of heterostyly.•The consistent association between style polymorphism and heteromorphic incompat-ibility points to ecological factors as drivers of the multiple evolution of style polymor-phism inLinum. Albeit based on limited evidence, we hypothesised that specialisedpollinators and lack of mating opportunities drive evolution of style polymorphismand loss of the polymorphism, respectively.