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Stigma shape shifting in sages (Salvia: Lamiaceae): hummingbirds guided the evolution of New World floral features

2022    Kriebel, Ricardo; Drew, Bryan T.; Gonzalez-Gallegos, Jesus G.; Celep, Ferhat; Antar, Guilherme M.; Pastore, Jose Floriano Barea; Uria, Rolando; Sytsma, Kenneth J.

A fundamental question in evolutionary biology is how clades of organisms exert influence on one another. The evolution of the flower and subsequent plant/pollinator coevolution are major innovations that have operated in flowering plants to promote species radiations at a variety of taxonomic levels in the Neotropics. Here we test the hypothesis that pollination by Neotropical endemic hummingbirds drove the evolution of two unique stigma traits in correlation with other floral traits in New World Salvia (Lamiaceae). We examined morphometric shapes of stigma lobing across 400 Salvia spp., scored presence and absence of a stigma brush across Salvia, and used a suite of phylogenetic comparative methods to detect shape regime shifts, correlation of trait shifts with BayesTraits and phylogenetic generalized least square regressions, and the influence of scored pollinators on trait evolution using OUwie. We found that a major Neotropical clade of Salvia evolved a correlated set of stigma features, with a longer upper stigma lobe and stigmatic brush, following an early shift to hummingbird pollination. Evolutionary constraint is evident as subsequent shifts to bee pollination largely retained these two features. Our results support the hypothesis that hummingbirds guided the correlative shifts in corolla, anther connective, style and stigma shape in Neotropical Salvia, despite repeated shifts back to bee pollination.