A remarkable case of pollinator/orchid coevolution and specificity

A science paper at last! Truth be told, I don’t come across many science papers that are both of general interest and that I can explain easily. But I do have several more in the queue.

A colleague sent me an old paper (from 2006), but its age does not diminish how spectacular the results are. And in short, the results are these: a group of 15 phenotypically similar (but probably not closely related) orchids in SW South Africa are pollinated by females of a single species of bee, which collects oil produced by the flowers and feeds it to their offspring.

This poses a problem, because orchids are pollinated by affixing sticky pollinia (sacs of pollen) collected from a flower of one species to the next flower of the same species. (The orchids in this group do not self-fertilize). With pollen sacs from 15 different orchid species sticking to a bee, how can a plant be sure that its own pollen gets transferred to another individual of the same species, rather than to another individual of a different species, in which case cross-species pollination would produce either inviable or maladapted hybrids?

The bees and orchids have solved this in a very clever way.

But let’s back up: the paper, from the American Journal of Botany, can be seen for free by clicking on the screenshot below, and the pdf is here.

The reason the author, Anton Pauw, gives for his 8-year investigation is that, he says, the “conventional wisdom” in botany is that it’s not adaptive for a bunch of flowers to depend on a single species of pollinator. That’s because if some environmental fluctuation or other contingency makes the pollinator rare (or even drives it extinct), the flowers wouldn’t get pollinated. This would imply that flowers should evolve to attract several species of pollinator, for those flowers that are generalists in this way are less likely to become rare or extinct themselves.

But this doesn’t seem to be the case in this group of 15 orchids, which, according to Pauw’s observation, come from three different genera (molecular phylogeny also suggests that they’re not each other’s closest relatives, though they look remarkably similar). Yet all are pollinated by a single bee, Rediviva peringueyi. This is in a genus called “long-legged oil bees.”

The flowers, as I said, look like each other, all produce oil that the bee collects, and all live in the same area, as well as flowering at the same time. As the author says,

Subgroups of similar plant species can be recognized within the extensive oil-bee pollination system. The one examined here includes 15 oil-secreting orchids that share the following syndrome of floral features: pale yellow-green flowers without extensive black markings; secretion of floral oil as a pollinator reward; characteristic pungent scent; flowering period 15 August to 25 October peaking in September; flower depth 5–8 mm (Fig. 1a–n). The species occur in close association with one another in the lowlands of the Cape Floral Region and include members of three genera (Pterygodium, Corycium, and Disperis). According to the pollination syndrome concept, the similar floral features of this group indicate a shared pollinator. My aim was to test this prediction through extensive field work.

Figure 1 below (click to enlarge; caption from paper) shows how similar the flowers are. The pollinating bee (R. poeringueyi, which I’ll henceforth call “the bee”) is shown in the middle. The arrows show where the pollinia of each orchid species gets attached:

The bees also collect pollen and nectar, too, but not from these orchids.  From these 15 orchids they take only flower oil (I had no idea it even existed), and do so by, as you can see in the photo below, gripping the plant with the bee’s middle and hindlegs and collecting the oil with modified forelegs. In the process (and of course this is why the flower produces oil and scent to attract the bee). During oil collection, the pollinia of the orchid, which is sticky, attaches to the bee’s body. That’s also shown in the photo below.

This, of course, raises the problem noted above. If a pollen sac from one of the 15 orchid species is stuck to the bee’s body, how can it be guaranteed to pollinate the same species of orchid, for there’s no guarantee that the next flower the bee visits will be from the same species. (All the orchids are, after all, flowering at the same time.)

The answer is the cool part of the story. Each orchid has evolved to stick its pollen to a different part of the bee’s body. And each orchid has its female parts placed so that the pollinia from its own species, stuck to a specific place on the bee’s body, will contact it’s own species-specific style (the female bit that gets the pollen for fertilization). Thus cross-pollination is prevented by the specificity of where the pollinia stick to the bee and bu the specific position of the female part of each orchid, which has evolved so, that when the bee collects oil, the right pollen will land on the right stigma.

Paux found this out by identifying the different pollina of the flowers (they have different shapes), and trapping wild bees to see where the pollinia of each species was stuck to the body. That’s what’s shown in the figure above: each letter corresponds to the orchids depicted around the edges, and the arrows show where on the bee’s body the pollinia from each species are stuck. Notice that they’re all different. Except for two, that is: the pollinia from orchids b and c, which both stick to the foretarsi of the bee’s middle legs.

Does this mean there’s cross-pollination between orchids b and c, which would be bad? No, because the pollinia of these two species are of different length, and the stigmas of the two orchids are placed so that each will get the pollen from the right species.

This is a remarkable example of specificity in pollen placement; I know of nothing similar! You can see below, in “b” and “c” of Fig. 3, that the pollen are stuck to very specific parts of the body. In “b”, the pollen of the flower Pterogodium cathlocium get attached to the bee’s “basistarsi” on the middle legs (the most distal part of the large leg tarsi), while the pollinia of the orchid Pterygodium volucris get attached to the ventral surface of the bee’s abdomen. The pollen sacs on the flowers have to be in very different places to accomplish this, and the bee has to collect oil in a specific position to get the pollinia stuck to the right spot.

Note that several types of evolution appear to be involved in this phenomenon:

a.) Convergent evolution of the different, unrelated orchids so that they develop a common scent, appearance, and “lip” that allows the bees to hang on while collecting oil.

b.) Divergent evolution of the orchids so that each evolves a lip and pollinia position that will stick its pollen to a previously uncolonized part of the bee’s body

c.) Possible evolution of the bee’s behavior so that it “knows” how to hold onto each species of flower to collect oil (this might not involve genetic evolution, but simply be due to learning).

So this is the cool way that fifteen different species of orchids can pollinate members of their own species, even if they’re all serviced by the same species of pollinator.  According to Pauw, though, this doesn’t solve the problem raised at the beginning: such specificity makes the whole system precarious—liable to collapse if anything happens to the pollinator. And indeed, he says that the degree of pollination of the orchid species vary strongly from year to year. So it goes.

Another aspect of this system is the possible extinction of the bee. In a sad ending, Pauw notes that the habitat for both orchid and bee is disappearing:

The biggest challenge in this study was the scarcity of suitable study sites. About 80% of lowland vegetation has already been transformed by urbanization and agriculture (Heijnis et al., 1999). What remains are scattered fragments of natural habitat, mostly less than 1 ha in size. In many of these fragments, the absence of R. peringueyi and repeated pollination failure in the entire guild was recorded. We have probably already lost the chance to understand the intriguing flowers of species such as P. cruciferum, which persists in fewer than five remnants of natural vegetation where they seldom, if ever, receive pollinator visits. In contrast with the pollination systems of the north temperate regions, which almost invariably involve several ecologically equivalent pollinator species (Waser et al., 1996; Fenster et al., 2004), the pollination system described here is dependent on a single insect species. This presents a challenge for conservation because of the low level of ecological redundancy means that the loss of R. peringueyi may trigger linked extinctions amongst the plants in the R. peringueyi pollination guild. It seems unlikely that the R. peringueyi pollination guild will persist in a modern, cultural landscape without unique conservation planning.

If the bee goes extinct, so will every one of these orchid species, for their reproduction depends on the insects. There’s a lot more to study here, and I’m hoping that they’re trying to save some habitat for both plant and insect.  Since pollination itself has been observed in only about five of these orchids, there’s a lot more observational work to be done. Further, the DNA analysis of the orchids, indicating that they are not a “monophyletic group” (i.e., not each other’s closest relatives) was rather crude, and that needs to be done using more modern methods. If they are not each other’s closest relatives, then we have a new and solid case of “convergent evolution” (unrelated species developing very similar traits).

h/t: Martim