Repeated and diverse losses of corolla bilateral symmetry in the Lamiaceae.

Background and Aims: Independent evolution of derived complex characters provides a unique opportunity to assess whether and how similar genetic changes correlate with morphological convergence. Bilaterally symmetrical corollas have evolved multiple times independently from radially symmetrical ancestors and likely represent adaptations to attract specific pollinators. On the other hand, losses of bilateral corolla symmetry have occurred sporadically in various groups, due to either modification of bilaterally symmetrical corollas in late development or early establishment of radial symmetry. Methods: This study integrated phylogenetic, scanning electron microscopy (SEM)-based morphological, and gene expression approaches to assess the possible mechanisms underlying independent evolutionary losses of corolla bilateral symmetry. Key Results: This work compared three species of Lamiaceae having radially symmetrical mature corollas with a representative sister taxon having bilaterally symmetrical corollas and found that each reaches radial symmetry in a different way. Higher core Lamiales share a common duplication in the CYCLOIDEA (CYC ) 2 gene lineage and show conserved and asymmetrical expression of CYC2 clade and RAD genes along the adaxial-abaxial floral axis in species having bilateral corolla symmetry. In Lycopus americanus , the development and expression pattern of La-CYC2A and La-CYC2B are similar to those of their bilaterally symmetrical relatives, whereas the loss of La-RAD expression correlates with a late switch to radial corolla symmetry. In Mentha longifolia , late radial symmetry may be explained by the loss of Ml-CYC2A , and by altered expression of two Ml-CYC2B and Ml-RAD genes . Finally, expanded expression of Cc-CYC2A and Cc-RAD strongly correlates with the early development of radially symmetrical corollas in Callicarpa cathayana . Conclusions: Repeated losses of mature corolla bilateral symmetry in Lamiaceae are not uncommon, and may be achieved by distinct mechanisms and various changes to symmetry genes, including the loss of a CYC2 clade gene from the genome, and/or contraction, expansion or alteration of CYC2 clade and RAD -like gene expression.