The Orchidaceae have a history of recurring convergent evolution in floral function as nectar production has evolved repeatedly from an ancestral nectarless state. Hobbhahn et al. study the South African orchid genus Disa and find that independent nectary evolution has involved both repeated recapitulation of secretory epidermis, which is present in the sister genus Brownleea, and innovation of stomatal nectaries. These contrasting nectary types and positional diversity within types imply weak genetic, developmental or physiological constraints in ancestral, nectarless Disa. With its morphologically diverse solutions to the problem of nectar production, Disa is a good example illustrating the contribution of functional convergence to phenotypic diversification, which probably also underlies the extensive diversity of nectary types and positions in the orchid family.
Valentine’s Day is coming, and many people are looking for the right flower to express their feelings, though it’s hard to beat a multi-coloured rose. But where do all the different sorts of flowers come from?
The Grant-Stebbins model suggests that pollinators drive speciation. Shifts in pollinators cause angiosperms (flowering plants) to adapt and form ‘ecotypes’ which then become new species. To someone like me, who is not a botanist, this is an appealing explanation. In reality it’s more complicated than that.
Pollinator-Driven Speciation is the subject of a recent special issue for Annals of Botany. I’ll be blogging about papers from the issue during the week. In their introductory paper for the issue, Van der Niet, Peakall and Johnson point out there’s plenty of evidence of floral adaptation to pollinators, and evidence at the large-scale of angiosperms diversifying with pollinators, but there’s a gap in the middle. How do you get from floral adaptation to speciation?
Van der Niet et al. identify four key factors in their paper. First you need to show that pollinators are selecting which plants get fertilised and which don’t. Next you need to show that this selection has consequences for floral traits. After this you’d need to look at the geographical context. What is it that causes you to find a certain plant here but not there? Finally, you’ll want to show that the pollinators are helping isolate populations so the differences between plant populations don’t spread back through the parent population.
Breaking down the problem really helps, because it means we can move from a general idea to some testable hypotheses. This is what the viewpoint paper does and each step is peppered with citations showing how each one of them can be tested with evidence. In the case of pollinator selection it’s possible to do direct experiments.
One of the most important factors in experimenting is that you also have to accept you may be wrong about something. In the conclusions Van der Niet et al. say the Grant-Stebbins model does a good job of explaining speciation, but there are some non-pollinator factors involved too. Strangely I think this is actually an excellent result for the model.
A model that explains everything risks being a just-so story. The fact it breaks down in places shows that scientists aren’t simply recording what they expect to see. However, the model breaking down doesn’t make it useless. The fact that it usually works means that when it does fail, it is pointing out that something really interesting and unexpected is going on. This is one of the most useful things a scientific model can do, take a lot of different observations and help you sort out what results are excitingly weird.
You can pick up the viewpoint paper that introduces the pollinator-driven speciation issue from the Annals of Botany.
Lycopodium obscurum has a subterranean, mycoheterotrophic gametophyte that nourishes the embryo for several years. An examination of an embryo in an underground gametophyte by Renzaglia and Whittier reveals a massive foot with ultrastructural variability comparable to that across major clades. The intergenerational zone in unlobed regions shows unidirectional transport of materials toward the foot. Lobed, more mature areas contain degenerated gametophyte cells that lack wall ingrowths and sporophytic transfer cells. They conclude that placental features in Lycopodium reflect a dynamic, invasive and long-lived foot, and the unique reorientation of all embryonic regions during development. Homoplasy in transfer cell appearance and location is explained by diverse patterns of embryology across archegoniates.
Repeated hybridizations and/or polyploidizations confound taxonomic classification and phylogenetic inference, and multiple colonizations at different time scales complicate biogeographic reconstructions. Pimentel et al. sequence three plastid and two nuclear DNA regions in 17 Anthoxanthum taxa in order to unravel the role of these processes in shaping the current structure and diversity of the genus. Variation of floral morphology in Anthoxanthum (sections Anthoxanthum and Ataxia) can be explained by a Miocenic hybridization event between lineages with one and three fertile florets. All diversification events in the genus except one are dated back to between the Late Pliocene and the Late Pleistocene. Africa was apparently colonized twice from two different sources, namely Europe and East Asia.
Stomatal structure is highly conserved across land plants – a symmetric pair of specialized guard cells delimits a central pore. However, when viewed from a developmental perspective, the patterning of the stomatal complex (the stoma and neighbouring cells) differs among taxa. Most hypotheses of stomatal evolution in angiosperms are based on comparative studies of mature stomata of both extant and fossil taxa, with a primary focus on three widely recognized stomatal types – anomocytic, paracytic and stephanocytic – which differ in the patterning of their neighbour cells.
Understanding evolutionary pathways requires a more explicit phylogenetic context than over-simplistic comparisons between dicotyledons (a non-monophyletic group) and monocotyledons. Such comparisons are most commonly exemplified by the model organisms Arabidopsis and rice, respectively. A recent paper in Annals of Botany presents a novel ultrastructural study of developing stomata in leaves of Amborella (Amborellales), Nymphaea and Cabomba (Nymphaeales), and Austrobaileya and Schisandra (Austrobaileyales), which represent the three earliest-divergent lineages of extant angiosperms. The authors show that similar mature stomatal phenotypes can result from contrasting morphogenetic factors. Loss of asymmetric divisions in stomatal development could be a significant factor in land plant evolution, with implications for the diversity of key structural and physiological pathways.
Self-pollination is often regarded as an evolutionary dead end, yet many selfers seem capable of retaining high adaptive potential. Andersson and Ofori perform experimental crosses within an initially self-sterile population of Crepis tectorum to produce an outbred and inbred progeny population, and find that a shift to selfing promotes adaptive potential for leaf morphology by increasing the overall genetic variance and by exposing potentially advantageous recessive alleles to selection. The results point to a positive role for inbreeding in phenotypic evolution, at least during or immediately after a rapid shift in mating system.
It is widely acknowledged that eukaryotic cells (you know, the ones with a membrane-bound nucleus and a variety of other membrane-bound organelles (cf. prokaryotes)) came to be so complex by a series of ‘mergers and acquisitions’ that saw a prokaryote-like cell internalise other, smaller ‘cells’ to gain organelles such as mitochondria and chloroplasts. That is the essence of the Serial Endosymbiotic Hypothesis/Theory. But have you ever wondered how long ago such events took place? Well, Patrick Shih and Nicholas Matzke have done so on our behalf .
Using ‘cross-calibrated phylogenetic dating of duplicated ATPase proteins’ (which are retained by mitochondria and chloroplasts and involved in energy production in both), the duo’s results suggest that primary plastid endosymbiosis (which eventually gave us plant cells) occurred approximately 900 Mya (millions of years ago), whereas mitochondrial endosymbiosis occurred around 1200 Mya. Interestingly, both authors contributed equally to this work, and both were PhD students at the time! I’d so like one of the authors to have done the mitochondria work, and the other to have been ‘responsible’ for chloroplasts; that would make for a pleasingly symmetrical, modern-day parallel to the 19th century’s Cell Theory, largely attributed to Schleiden (‘botanist’) and Schwann (‘zoologist’). Way to go, gentlemen!
[Please don’t construe Mr Cuttings’ comments about putative parallels with Schleiden and Schwann to mean that only animal cells have mitochondria, and only plant cells have chloroplasts; plant cells can contain both (yes, so they are better than animals…)! – Ed.]
When it comes to carnivorous plants it’s Venus Flytraps that get the most attention, with their snapping jaws. Bladderworts have stunningly fast traps. Sundews glisten and coil around their prey. Pitcher plants like the Nepenthaceae in contrast don’t seem to do much. It looks like they’re just sitting there, waiting for gravity to do the work, almost like couch potatoes. In fact there’s a lot going on, as a paper from next month’s Annals of Botany shows.
Jonathan A. Moran, Laura K. Gray, Charles Clarke and Lijin Chin have written a paper Capture mechanism in Palaeotropical pitcher plants (Nepenthaceae) is constrained by climate (you can read it for free) that not only looks at what pitcher plants do, but also where they do what do. And they’ve looked at a lot of plants – almost 2000 populations of over 90 different species. So what is it that pitcher plants are doing?
Angiosperms, the flowering plants, are the astonishingly diverse. But what drives the selection pressures to create this diversity? One explanation is the Grant-Stebbins model. This model looks at pollination as a selection process. Many flowers need pollinators. If there are no pollinators, the plants don’t get pollinated and they have no offspring. It means that plants have to live where the ranges of their pollinators are. Plants that evolve to pull in more pollinators will have more success. Flowers are therefore constantly evolving to attract visitors.
It’s an interesting idea, but how do you test it?
Newman, Anderson and Johnson investigated the South African plant Disa ferruginea for their paper ‘Flower colour adaptation in a mimetic orchid‘. This is a clever piece of work based on a mimetic orchid. Disa ferruginea doesn’t waste time producing a reward for visiting insects, but this means there’s no obvious reason for a pollinator to want to visit. Instead D. ferruginea looks like the flowers of other nectar producing plants. What makes D. ferruginea odd is that it doesn’t always look like the same plant. In the west it has red flowers. In the east it’s orange.
Newman et al. thought this might be that pollinators were selecting the plants that looked most like the nectar bearing species, so they conducted an experiment. They swapped some orchids, so some orange orchids were found in the west, and some red orchids were moved to the east. Then they watched to see what happened.
The only insect that pollinates D. ferruginea is a butterfly Aeropetes tulbaghia. Sure enough they found that in the west they tended to ignore the orange plants and stick with the red orchids. In the east they skipped over the red orchids but stuck with the orange flowers. In both sites it was the orchids that looked most like the reward-bearing plants that attracted pollinators, so here was proof that pollinator selection was happening.
I suppose the follow-up experiment would be to relocate butterflies from one range to another, but I’ve no idea how you’d manage to fit them with radio transmitters to track them.
This isn’t the only test of Grant-Stebbins.
Ellis and Johnson (the same Johnson mentioned above) have published a paper ‘The Evolution of Floral Variation Without Pollinator Shifts in Gorteria Diffusa (Asteraceae)‘. Gorteria Diffusa is a South African daisy that’s usually pollinated by the bee fly Megapalpus capensis. Ellis and Johnson found fourteen different varieties of G. Diffusa. Each of the forms seems to be inherited, not a plastic adaptation to the environment, but they couldn’t find fourteen different pollination scenarios. If pollination isn’t the selective force, what is going on? Ellis and Johnson point to other work that argues that there’s more to plant survival than pollination. For example once you have the seeds you have to ensure that at least some of them get past predators to germinate. Also, while you want a flower to look tasty to a visiting pollinator, do you really want to attract larger herbivores that will simply eat the flower?
It’s clearly a problem that needs more research, and there’s a whole special issue on pollinator-driven speciation on the way from Annals of Botany. The earliest papers are available as advanced access to subscribers including ‘Do pollinator distributions underlie the evolution of pollination ecotypes in the Cape shrub Erica plukenetii?‘ by Van der Niet, Pirie, Shuttleworh, Johnson and Midgley. Yes, the same Johnson.
Erica plukenetii is a shrub that grows waist-high, if your waist is typically 90cm above the ground. You can find it on the slopes of South African mountains, but you’ll find it with more than one pollinator. The typical E. plukenetii has a corolla (set of petals) of medium length. These are pollinated by the Orange-breasted sunbird (Anthobaphes violacea). A sunbird is a big like a hummingbird in that it’s a small nectar-feeding bird. A difference is that sunbirds tend to perch to feed instead of hovering.
The Orange-breasted sunbird is not the only pollinator of E. plukenetii. In the north of their range the plants are pollinated by Malachite sunbirds (Nectarinia famosa). Malachite sunbirds have a longer bill and the E. plukenetii in this region have longer corollas. In the centre of their range there’s also a shorter corolla variety of E. plukenetii and this is not bird pollinated. Instead it’s pollinated by a moth. These means there are three ways to pollinate E. plukenetii and they seem to have developed from the middle form. How does this fit with the Grant-Stebbins model?
Van der Niet et al. argue that the longer corolla plant fits the Grant-Stebbins model very well. As you go north Orange-breasted sunbirds become rarer and Malachite sunbirds more common, so the flowers better suited to the Malachite sunbirds will produce more offspring. Here pollinator selection makes sense. What about the short-corolla plants?
These are in the middle of the range, but here there are already plenty of Orange-breasted sunbirds, so they didn’t need to change to attract them. In fact, they’ve evolved to move away from the pollinators. This contradicts the Grant-Stebbins model. Van der Niet et al. suggest that other pressures must have an influence, and compare the bird pollinated E. plukenetii, found on mountainsides with the moth-pollinated E. plukenetii, found on flatter land. The moth-pollinated plants have slender branches that don’t support birds well. If this is necessary to colonise the flats, then it’s the habitat that changes the pollinator for the plant, instead of the pollinator defining the plant’s habitat.
It seems likely that it’s not just pollinators that select plants, but that plants can also select pollinators. One example is the paper ‘Domestication of cardamom (Elettaria cardamomum) in Western Ghats, India: divergence in productive traits and a shift in major pollinators‘ by Kuriakose, Sinu and Shivanna. Domesticating crops brings about a lot of changes. In the case of cardamom one change is there are flowers around for a lot longer than in the wild. For wild cardamom the pollinators tend to be solitary bees. For domesticated cardamom the flowers attracted social bees, the Purple sunbird and the Little Spiderhunter, a bird which – despite its name – is fond of nectar. The change in floral display seems to attract an entirely different kind of pollinator. Wild and cultivated cardamom don’t seem to share pollinators, despite being compatible with each other.
What seems to be happening is that where selection can occur, it will occur. While there are many scenarios where that can happen, like herbivory or habitat, competition for pollinators is in some cases a major factor in driving the evolution of plants.
The Annals of Botany special issue on pollinator-driven speciation is due out early 2014, with subscribers getting early access to some papers now. The issue will become free-access in 2015.
Ellis A.G. & Johnson S.D. (2009). The evolution of floral variation without pollinator shifts in Gorteria diffusa (Asteraceae), American Journal of Botany, 96 (4) 793-801. DOI: 10.3732/ajb.0800222 (free access)
Kuriakose G., Sinu P.A. & Shivanna K.R. (2008). Domestication of cardamom (Elettaria cardamomum) in Western Ghats, India: divergence in productive traits and a shift in major pollinators, Annals of Botany, 103 (5) 727-733. DOI: 10.1093/aob/mcn262
Newman E., Anderson B. & Johnson S.D. (2012). Flower colour adaptation in a mimetic orchid, Proceedings of the Royal Society B: Biological Sciences, 279 (1737) 2309-2313. DOI: 10.1098/rspb.2011.2375 (free access)
Van der Niet T., Pirie M.D., Shuttleworth A., Johnson S.D. & Midgley J.J. Do pollinator distributions underlie the evolution of pollination ecotypes in the Cape shrub Erica plukenetii?, Annals of Botany, DOI: 10.1093/aob/mct193 (subscription access till 2015)
I’ve been catching up with blog posts from Botany 2013.
One session that grabbed a lot of attention was “Yes, Bobby, Evolution is Real!“, a session that tackled encroaching attempts to inject selected religious viewpoints over others in US science classes. The session’s title was pointed, given that New Orleans is in Louisiana, where the state’s governor is Bobby Jindal. It was described by the Huffington Post as The Day That Botany Took on Bobby Jindal by Just Being Itself. Uh,oh! Botanists laugh at LA legislators who don’t like evolution, says the Phytophactor. Honest Ab notes that beyond that one session there was Evolution throughout the Botany 2013 Meetings, because that’s how plants get things done.
A search of the #BOTANY2013 hashtag on Twitter might still prove useful though as new tweets keep coming and some look very helpful.