Sex and the Catasetinae (Darwin’s favourite orchids)

• We investigated the evolution of sexual systems in the orchid subtribe Catasetinae.
• Maximum Likelihood and Bayesian methods were used to reconstruct ancestral states.
• Environmental sex determination (ESD) evolved three times within Catasetinae.
• Evolution of ESD and protandry is correlated from a phylogenetic prospective.
• A evolutionary scenario of protandry and ESD in orchids is for first time described.

Two sexual systems are predominant in Catasetinae (Orchidaceae), namely protandry (which has evolved in other orchid lineages as well) and environmental sex determination (ESD) being a unique trait among Orchidaceae. Yet, the lack of a robust phylogenetic framework for Catasetinae has hampered deeper insights in origin and evolution of sexual systems. To investigate the origins of protandry and ESD in Catasetinae, we sequenced nuclear and chloroplast loci from 77 species, providing the most extensive data matrix of Catasetinae available so far with all major lineages represented. We used Maximum Parsimony, Maximum Likelihood and Bayesian methods to infer phylogenetic relationships and evolution of sexual systems. Irrespectively of the methods used, Catasetinae were monophyletic in molecular phylogenies, with all established generic lineages and their relationships resolved and highly supported. According to comparative reconstruction approaches, the last common ancestor of Catasetinae was inferred as having bisexual flowers (i.e., lacking protandry and ESD as well), and protandry originated once in core Catasetinae (comprising Catasetum, Clowesia, Cycnoches, Dressleria and Mormodes). In addition, three independent gains of ESD are reliably inferred, linked to corresponding loss of protandry within core Catasetinae. Thus, prior gain of protandry appears as the necessary prerequisite for gain of ESD in orchids. Our results contribute to a comprehensive evolutionary scenario for sexual systems in Catasetinae and more generally in orchids as well.

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