Resin Midges, Basal Angiosperms, and a Strange Pollination Syndrome


When we try to talk about clades that are "basal" or "sister" to large taxonomic groups, your average listener either consciously or unconsciously thinks "primitive." Primitive has connotations of something that under-developed or unfinished. This is simply not the case. Take, for instance, a family of basal angiosperms called Schisandraceae.

This family is nestled within the order Austrobaileyales, which, along with a small handful of other families, represent the earliest branches of the angiosperm family tree still alive today.  To call them primitive, however, would be a serious misnomer. Because they diverged so early on, these lineages represent serious success stories in flowering plant evolution, having survived for hundreds of millions of years. Instead, we must think of them as fruitful early experiments in angiosperm evolution.

Floral morphology of and interaction between midge and their larvae (white arrows) in Illicium dunnianum

Still, the proverbial proof is in the pudding and if there was any sort of physical evidence one could put forth to remove our hierarchical prejudices about the taxonomic position of these plants, it would have to be their bizarrely specific pollination syndromes.  Members of the family Schisandraceae have entered into intense relationships with a group of flies known as midges and their interactions are anything but primitive. 

We will start with two species of plant native throughout parts of Asia. Meet as Illicium dunnianum and Illicium tsangii. More will be familiar with this genus than they may realize as Illicium gives us the dreaded star anise flavor our grandparents liked to sneak into our cookies as kids (but I digress). These particular species, however, have more to offer the world than flavoring. They are also very important plants for a group of gall midges in the genus Clinodiplosis.

The midges cannot reproduce without I. dunnianum or I. tsangii. You see, these midges lay their eggs within the flowers of these plants and, in doing so, end up pollinating them in the process. At first glance it may seem like a very one-sided relationship. Female midges deposit their eggs all along the carpels packed away inside large, fleshy whorl of tepals. As the midges crawl all over the reproductive organs looking for a suitable place to lay, they inevitably pick up and deposit pollen. 

Floral morphology and interaction between midge larvae (white arrows) in  Illicium tsangii

This is not the end of this relationship though. After eggs have been deposited, something strange happens to the Illicium flowers. For starters, they develop nursery chambers around the midge larvae. Additionally, their tepals begin producing heat. Enough heat is produced to keep the nursery chamber temperature significantly warmer than the ambient air temperature. What's more flower heating intensifies throughout the duration of fruit development. It was originally hypothesized that this heating had something to do with floral odor volatilization and seed incubation, however, experiments have shown that at least seed development in these two shrubs is not influenced by floral heat in any major way. The same cannot be said for the midge larvae. 

As the flowers mature and give way to developing seeds, the midge larvae are hard at work feeding on tiny bits of the flowers themselves. When researchers looked at midge larvae development on these Illicium species, they found that they were completely dependent upon the floral heat for survival. Any significant drop in temperature caused them to die. Essentially, the plants appear to be producing heat more for the midges than for themselves. It may seem odd that these two plants would invest so much energy to heat their flowers so that midge larvae feeding on their tissues can survive but such face-value opinions rarely stand in ecology.

One must not forget that those larvae grow up to be adult midges that will go on to pollinate the Illicium flowers the following season. Although the plants are taking a bit of a hit by allowing the larvae to develop within their tissues, they are nonetheless ensuring that enough pollinators will be around to repeat the process again. If that wasn't cool enough, the relationship between each of these plants and their pollinators are rather specific and the authors of at least one paper believe that the midges that pollinate each species are new to science. 

Now, if I haven't managed to convince you that this angiosperm sister lineage is anything but primitive, then let's take a look at another genus within the family Schisandraceae that have taken this midge pollination syndrome to the next level. This story also takes place in Asia but instead involves a genus of woody vines known as Kadsura

Like the Illicium we mentioned earlier, a handful of Kadsura species rely on midges for pollination. The way in which they go about maintaining this relationship is a bit more involved. The midges that are attracted by Kadsura flowers are known as resin midges and their larvae live off of plant resins. The flowers of Kadsura are another story entirely. They are as odd as they are beautiful. 

Flowers, pollinators ,and their larvae (white arrows) in  Kadsura heteroclita .

Flowers, pollinators ,and their larvae (white arrows) in Kadsura heteroclita.

In male flowers, stamens are arranged in dense, cone-like structures called androecia whereas the female flowers contain a compact shield-like structure with the uppermost part of the stigma barely emerging. This is called a gynoecium. Even weirder, the male flowers of one particularly strange species, Kadsura coccinea, produce large, swollen inner tepals. 

Once Kadsura flowers begin to open, visiting midges are not far behind. Male flowers seem to attract more midges than female flowers and it is thought that this has to do with varying amounts of special attractant chemicals produced by the flowers themselves. Regardless, midges set to work exploring the blooms with males looking for mates and females looking for a place to lay their eggs. 

When a suitable spot has been found, females will deposit their eggs into the floral tissues with their ovipositor. The wounded plant tissues immediately begin producing resin, not unlike a wounded pine tree. In the case of K. coccinea, it would appear that the oddly swollen tepals are specifically targeted by female midges for egg laying. They too produce resin upon having eggs laid within. 

The oddball flowers of Kadsura coccinea showing swollen tepals.

The function of plant resins in many cases are to fight off pathogens. From beetles to fungi, resin helps plug up and seal off wounds. This does not seem to be the case in the Kadsura-midge relationship though. The so-called "brood chambers" within the floral tissues go on producing resin for upwards of 6 days after the midge eggs were laid. Eventually the floral parts whither and drop off but the midge larvae seem to be quite happy in their resin-filled homes. 

As it turns out, the resin midge larvae feed on the viscous resin as their sole food source. Instead of trying to ward off these pesky little insects, the plants seem to be encouraging them to raise their offspring within! Just as we saw in the Asian Illicium, these Kadsura vines seem to be providing brood sites for their pollinators. Also, just as the Illicium-midge relationship thought to be species specific, each species of Kadsura appears to have its own specific species of resin midge pollinator! K. coccinea even goes as far as to produce tepals specifically geared towards raising midge larvae, thus keeping them away from their more valuable reproductive organs. In return for the nursery service, Kadsura have their pollinators all to themselves.

Pollination mutualisms in which plants trade raising larvae for pollen transfer are extremely derived and some of the most specialize plant/animal interactions on the planet. To find such relationships in these basal or sister lineages is living proof that these plants are anything but primitive. In the energy-reproductive investment trade-off, it appears that ensuring ample pollinator opportunities far outweighs the cost of providing them with nursery chambers. It is remarkable to think just how intertwined the relationships between these plants and there pollinators truly are. Take that, plant taxonomic prejudices! 

Photo Credits: [1] [2]

Further Reading: [1] [2] 


The Aposematic Gall Hypothesis

Maple eyespot gall (left) and the grape tumid gall (right)

Maple eyespot gall (left) and the grape tumid gall (right)

If you spend any time around plants you will have undoubtedly come across a gall. In fact, once you know what to look for you quickly realize that galls are everywhere. They come in many different shapes and sizes and they vary as much as the species you will find them on. Galls are abnormal growths on plant tissues and their causes range from bacteria, fungi, and nematodes to insects and mites. Most of the galls we regularly encounter are caused by insects. 

You can think of galls as a type of edible nursery chamber. A female insect will lay her eggs in the tissue of the plant and chemicals released by the eggs and subsequently the developing larvae trigger abnormal tissue growth in the plant. Every detail of each gall you see is the result of the insect housed inside, which has led some authors to consider gall formation a literal extension of the insect phenotype. Without the chemicals released by the developing insects, the plant would not form such elaborate growths.

Lime nail gall ( Eriophyes tiliae )

Lime nail gall (Eriophyes tiliae)

As mentioned, galls act as an edible nursery chamber. Not only does the developing larvae gain physical protection, they also consume the swollen plant tissues on the inside of the gall. Despite the attention galls have received in the literature, very few studies have touched on one fact of gall ecology that becomes quite obvious to the casual observer - most of them are very conspicuous.

Oak apple gall (Cynipidae)

Oak apple gall (Cynipidae)

The shape and coloration of different kinds of gall causes them to really stand out against the background vegetation. Why would a structure meant to protect the developing insect inside be so easy to spot? A handful of interesting hypotheses have been put forth to explain this phenomenon. For starters, the chemical compounds that give many galls their distinctive coloration are the result of hijacked plant pigments such as carotenoids, anthocyanins, as well as tannins and other phenolic compounds. These are thought to protect the insect inside. This certainly plays a role, but we will come back to that in a minute.

Cynipid gall ( Diplolepis polita )

Cynipid gall (Diplolepis polita)

Still, one would think being so strikingly obvious would have some serious drawbacks. Predators and parasitoids alike could easily hunt down a bright red gall. Even if potential predators can't see color, the outlandish shape of many galls certainly makes them stand out. There is another hypothesis that gets right to the core of this. Simply put, it is thought that the conspicuousness of galls serves as a warning to potential predators that eating them would be a mistake. In other words, galls very well may be aposematic. 

You will be most familiar with aposematic coloring in bees and wasps. Bright colors such as red or yellow contrasted against a strikingly different colored background serve as a warning to anything that might be thinking of taking a bite. "Stay away, I will hurt you" is the gist of the message. The bright coloration and often outlandish shape of galls coupled with the defensive compounds mentioned above may be sending a signal to herbivores, predators, and parasites to stay away or risk injury or illness. Being easy to find also makes galls easier to remember and a bad experience with one gall may make a bird think twice before messing with one again. In this way, the insects inside can go unmolested until it matures. 

Obviously there are many caveats to this idea. Certainly not all galls fall under this umbrella. The researchers behind this hypothesis have outlined a series of predictions that are thought to promote the evolution of aposematism as a strategy. What's more, this hypothesis will need to be tested on many different types of galls in many different habitats with many different potential predators if it is to hold up. Still, it is an interesting idea worth investigating. One can see the potential here. 

Photo Credits: [1] [2] [3]

Further Reading: [1]