Staminal evolution in the genus Salvia (Lamiaceae): molecular phylogenetic evidence for multiple origins of the staminal lever

Abstract

Background and aims: The genus Salvia has traditionally included any member of the tribe Mentheae (Lamiaceae) with only two stamens and with each stamen expressing an elongate connective. The recent demonstration of the non-monophyly of the genus presents interesting implications for staminal evolution in the tribe Mentheae. In the context of a molecular phylogeny, the staminal morphology of the various lineages of Salvia and related genera is characterized and an evolutionary interpretation of staminal variation within the tribe Mentheae is presented.

Methods: Two molecular analyses are presented in order to investigate phylogenetic relationships in the tribe Mentheae and the genus Salvia. The first presents a tribal survey of the Mentheae and the second concentrates on Salvia and related genera. Schematic sketches are presented for the staminal morphology of each major lineage of Salvia and related genera.

Key results: These analyses suggest an independent origin of the staminal elongate connective on at least three different occasions within the tribe Mentheae, each time with a distinct morphology. Each independent origin of the lever mechanism shows a similar progression of staminal change from slight elongation of the connective tissue separating two fertile thecae to abortion of the posterior thecae and fusion of adjacent posterior thecae. A monophyletic lineage within the Mentheae is characterized consisting of the genera Lepechinia, Melissa, Salvia, Dorystaechas, Meriandra, Zhumeria, Perovskia and Rosmarinus.

Conclusions: Based on these results the following are characterized: (1) the independent origin of the staminal lever mechanism on at least three different occasions in Salvia, (2) that Salvia is clearly polyphyletic, with five other genera intercalated within it, and (3) staminal evolution has proceeded in different ways in each of the three lineages of Salvia but has resulted in remarkably similar staminal morphologies.

Fig. 1.

Stylized representation of the flower and lever mechanism of pollination of a hypothetical member of Salvia subgen. Calosphace (Salvia clade II). A flower prior to the activation of the lever mechanism (A). The pollinator enters the flower and activates the lever mechanism (B), depositing pollen on the head of the pollinator. (C) A ‘birds-eye’ view of the flower, with the fused posterior branches of the connective blocking access to the nectar at the base of the corolla (sketch by Cody Williams).

Fig. 2.

The generalized trend in stamen morphology seen within tribe Mentheae leading to that seen in Salvia. Shaded areas represent connective tissue. Step 2 (the functional loss of two of the four stamens) has apparently happened only once in the Salvia clade. The progression from step 2 to step 5 has happened on at least three independent occasions in the Salvia clade. Anterior thecae are on the top of each sketch, and the posterior thecae, which become entirely aborted and fused in step 5, are on the bottom of each sketch.

Fig. 3.

The ‘Mentheae-wide’ analysis. A three-region DNA, combined parsimony analysis of the chloroplast regions trnL-F, psbA-trnH and the nuclear rDNA ITS. Strict consensus of 2094 equally parsimonious trees of length 1737 steps. Bootstrap values above 50 % are shown above the branches. In addition to all Salvia, the ‘Salvia clade’ includes the genera highlighted in bold.

Fig. 4.

The ‘Salvia clade’ analysis. A two-region DNA, combined parsimony analysis of the chloroplast region trnL-F and the nuclear rDNA ITS. Strict consensus of over 100 000 equally parsimonious trees of 1489 steps. Bootstrap values above 50 % are shown above the branches. Stamen types corresponding to those in Fig. 5 and Table 2 are shown. Non-Salvia genera are highlighted in bold.

Fig. 5.

A summary of the cladogram shown in Fig. 4, with representations of the stamen types found in each clade. Shaded areas of the sketches represent connective tissue. Grey lines in the cladogram represent branches in which significantly elongate connectives are seen. Dashed lines in the cladogram represent lineages in which a lever mechanism is found. Total abortion of the posterior thecae and total fusion of the posterior thecae occurs only in stamen types B, E and N. Species numbers were hypothesized based on subgeneric groups suggested in the literature (Epling, 1938, ; Hedge 1974, 1982a, b). The two taxa with asterisks represent taxa not possessing the ‘typical’ stamen type A, and both possessing stamens with no expressed posterior thecae.

Fig. 6.

Hypothesis of evolutionary progression in the independent origin of the three different staminal lever mechanisms found in the tribe Mentheae. This figure represents a modification and revision of Himmelbaur and Stibal's (1934) original interpretation of staminal evolution in Salvia. The three lever mechanisms (Salvia clade I, clade II and ‘clade III’) are homologous in that they are derived from the connective tissue of the stamen (shaded in this figure), but have been independently derived and are morphologically distinct from one another.