Wednesday, 15 February 2017

The Clever Lever

Since early times Salvia has been related to healing problems in human health; its very scientific name derives from the Latin salvus which translates to safe referring to its medicinal properties. In the Americas, Salvia is known not only for its medicinal but also for spiritual properties. For instance, Salvia divinorum (also known as sage of the seers) is popular for its use in shamanism by the Mazatecs. Traditionally it is used during spiritual healing sessions, when the shamans need to go deep in the supernatural world to discern the cause of the patient’s state. After consuming the herb, the shaman travels in visionary states of consciousness that will concede the steps to cure the patient. Believe it or not, it definitely sounds like a fascinating experience. But as a flower morphologist, there are some other particularities that I would also classify as fascinatingly interesting. And yes, I am obviously talking about floral structures, one in particular that has changed the whole evolutionary path of Salvia.

Traditional Mazatec Shaman ceremony with Salvia divinorum

Salvia is a widely distributed genus of nearly 1000 species, all of which share a unique pollination strategy known as the staminal lever mechanism. Like almost any member of Lamiales, the number of stamens varies from two to five in different species. In fact, there is a tendency in this group for a reduction or complete absence of the posterior stamens (i.e., stamens at the top) as a consequence of bilateral symmetry (learn more here). However this doesn’t seem to affect pollination efficiency, and there are many examples of pollination strategies where flowers tend to package their pollen or develop complex structures to restrict pollen collection in a single flower visit.

Flower diversity in Salvia 

Sources: Flickr (1, 3, 4, 5), Flora-on (2), Flowers in Israel (6)

In Salvia, flowers have only two stamens, and the stamen’s connective which separates the thecae of each anther becomes elongated. This elongation of the stamen connective varies in length from species to species, and it is this abnormal length of the stamen connective that allows the formation of a lever mechanism. And this lever mechanism is considered to be a key innovation since it created a very effective pollination artifice for which Salvia is best known.

But how exactly does this mechanism work? 

What happened in the course of evolution of the Salvia androecium is that the posterior thecae of each stamen became unfertile and both fused together, creating a structure called the lower lever arm. This structure is centrally located on the base of the corolla’s entrance, whereas the fertile thecae stay on the upper lip of the corolla. When a nectar seeking pollinator enters the flower, it compresses the lower lever arm, and the fertile thecae immediately deposit the pollen on the back of the pollinator.

Evolution of the staminal lever in Salvia
1 – Ancestral state of androecium morphology in Salvia (generalized trend within tribe Mentheae); 2 – Funcional loss of the posterior stamens; 3 and 4 – Elongation of connective tissue between both thecae; 5 – functional abortion and fusion of both posterior thecae, the lower lever arm is formed!; Picture: Walker & Sytsma 2006 

The pollen deposition systems are highly precise in Salvia species with a high level of specialization to different pollinators, and even to different parts of the body of the same species of bee (learn more here). This has driven the evolution and radiation of the entire genus. This radiation is the reason why the lever mechanism is considered to be a key innovation – because it lead to a boom of diversification.

Examples of pollen deposition systems in Salvia
A: Pollen transfer in Salvia pratensis; top picture is a scheme of the mechanism of the lever; bottom left picture shows a pollinator entering a young flower to access the nectar, pushing the lever (in black) and triggering pollen loading on its back; bottom right picture show a later stage of the same flower, in which the style (in black) takes the position of the stamens (not represented here) and the insect deposits the pollen collected in another flower of the same species on the stigma of this one; Picture: Claßen-Bockhoffet al 2004B: Pollen transfer in Salvia lanceolata – to access the nectary (n), the pollinator (Nectarinia chalybea) pushes the lever arms (pc) and the thecae (t) at the anterior connective arms (ac) move down to deposit the pollen on the bird’s head, j is the joint between filament and connective that enable this movement; Picture: Wester & Claßen-Bockhoff 2007

Of course, as all Salvia’s share this unusual pollination syndrome that relies on such a complex staminal structure, botanists used to believe that Salvia only speciated after the evolution of the staminal lever. That Salvia was monophyletic (i.e. shared a common ancestor) and the staminal lever evolved only once. But it’s a trap! Recent studies have actually revealed that Salvia is actually polyphyletic (i.e., the lever arm evolved many times). Thus, what we classified as a single genus in the past is actually four distinct evolutionary lineages that have evolved in parallel (learn more here). Though I still find it hard to believe such structure evolved so many times, this proves we botanists, have alot to learn about plant evolution. But isn’t it wonderful to know there is still so much to learn?!