Towards a global perspective for Salvia L: Phylogeny, diversification, and floral evolution

Abstract

Premise of this studySalvia is the most species-rich genus in Lamiaceae, encompassing approximately 1000 species distributed all over the world. We sought a new evolutionary perspective for Salvia by employing macroevolutionary analyses to address the tempo and mode of diversification. To study the association of floral traits with speciation and extinction, we modeled and explored the evolution of corolla length and the lever-mechanism pollination system across our Salvia phylogeny.MethodsWe reconstructed a multigene phylogeny for 366 species of Salvia in the broad sense including all major recognized lineages and numerous species from Iran, a region previously overlooked in studies of the genus. Our phylogenetic data in combination with divergence time estimates were used to examine the evolution of corolla length, woody vs. herbaceous habit, and presence vs. absence of a lever mechanism. We investigated the timing and dependence of Salvia diversification related to corolla length evolution through a disparity test and BAMM analysis. A HiSSE model was used to evaluate the dependency of diversification on the lever-mechanism pollination system in Salvia.Key ResultsBased on recent investigations and classifications, Salvia is monophyletic and comprises ∼1000 species. Our inclusion, for the first time, of a comprehensive sampling for Iranian species of Salvia provides higher phylogenetic resolution for southwestern Asian species than obtained in previous studies. A medium corolla length (15-18mm) was reconstructed as the ancestral state for Salvia with multiple shifts to shorter and longer corollas. Macroevolutionary model analyses indicate that corolla length disparity is high throughout Salvia evolution, significantly different from expectations under a Brownian motion model during the last 28 million years of evolution. Our analyses show evidence of a higher diversification rate of corolla length for some Andean species of Salvia compared to other members of the genus. Based on our tests of diversification models, we reject the hypothesis of a direct effect of the lever mechanism on Salvia diversification.ConclusionsUsing a broader species sampling than previous studies, we obtained a well- resolved phylogeny for southwest Asian species of Salvia. Corolla length is an adaptive trait throughout the Salvia phylogeny with a higher rate of diversification in the South American clade. Our results suggest caution in considering the lever-mechanism pollination system as one of the main drivers of speciation in Salvia.

The genetic mechanisms underlying the convergent evolution of pollination syndromes in the Neotropical radiation of Costus L.

“…Our diversification analysis indicated no significant association between labellum shape and diversification ( Supplementary Table 5 ) with the CID4 model of HiSSE showing the smallest AIC value. On one hand the lack of association is somewhat surprising since other studies have shown a strong association with diversification and traits important for pollination such as with floral pigments ( Smith et al, 2010 ; Smith and Goldberg, 2015 ; Landis et al, 2018 ) and pollination trapping ( Xue et al, 2020 ), corolla length ( Moein et al, 2021 ), and corolla shape ( Fernandez-Mazuecos et al, 2013 ). However, other traits important for pollination appear to be decoupled with diversification such as the lever mechanism in Salvia ( Moein et al, 2021 ).…”

“…On one hand the lack of association is somewhat surprising since other studies have shown a strong association with diversification and traits important for pollination such as with floral pigments (Smith et al, 2010;Smith and Goldberg, 2015;Landis et al, 2018) and pollination trapping (Xue et al, 2020), corolla length (Moein et al, 2021), and corolla shape (Fernandez-Mazuecos et al, 2013). However, other traits important for pollination appear to be decoupled with diversification such as the lever mechanism in Salvia (Moein et al, 2021). Pollinator-mediated selection likely acts on more than one trait at a time to impact diversification, as observed by O'Meara et al (2016), who found that the presence of a corolla, bilateral symmetry, and reduced stamen number synergistically act as key innovations to double diversification rates.…”

“…The possibility of both specialized pollination and of frequent shifts in pollination syndromes has been associated with increased opportunities for reproductive isolation ( Serrano-Serrano et al, 2017 ; Fragoso-Martínez et al, 2018 ) and higher diversification rates ( Lagomarsino et al, 2016 ; Xue et al, 2020 ). However, in some lineages there is not a clear association between phenotypic traits important for pollination or reproductive mode and rates of diversification ( Landis et al, 2018 ; Moein et al, 2021 ).…”