Wednesday, March 5, 2014

Taste And Be Tasted – Fair Is Fair

Biology concepts – metamerism, tagmentizaton, taste, arthropods, receptor, parasitism

Carbonated sodas come in all flavors, but across all cultures, it is
the carbonation that is the same. Mauby is a tree bark flavored
soda sold in the West Indies islands of Bermuda, Trinidad and the
like. On the left is a bird’s nest/white fungus soda sold in Vietnam.
I don’t think it includes the bird.
There is no doubt that humans love the taste of carbonated sodas. There are as many flavors as you can imagine, but the common element among them is the infusion of carbon dioxide (CO2). Do you taste the carbon dioxide or is it important for some other reason?

Many insects will tell you that it’s the CO2 that makes the difference. Fruit flies, mosquitoes, ticks and other insects can taste CO2 on surfaces and in the air. For mosquitoes and ticks, tasting CO2 helps them find food. These are hematophagous (blood-eating) organisms, and they find their victims by flying upstream along their exhaled CO2 and the CO2 that is exuded from their skin.

Even more amazing, fruit flies and other insects taste the increased CO2 that stressed (injured, diseased) flies emit. They may avoid other insects that are dying so they won’t be near disease or danger. In other insects, they may follow it to animal carcasses - their buffets. In either case, the insects can actually taste death.

But are they tasting CO2? It’s a gas, and we have said that gases are detected and perceived by smell, not taste (except for us and DMS). It turns out that CO2 sensation is really an exception. A 2007 paper from John Carlson’s group showed that the receptor heterodimer (hetero = different, and dimer = two different proteins) is made of GR21a and GR63a, two gustatory proteins (hence the GR in the name).

However, the two taste receptors are located on olfactory neurons. The signal is detected by taste signaling on a smell neuron, and the signals are then sent to the smell portion of the brain! This may be one of the biggest exceptions in all of taste science, and it’s the insects that have it and use it.

For insects to accomplish many different tasks with taste, it helps to have the taste receptors in specific places. Catfish had them all over their body, but that’s not very specific. In insects they are found in distinct places, and may have distinct functions.

The shrimp is a good example to show metamerism in arthropods.
All the parts are just reiterations of the same subunit. Some kept
their appendages, and some changed them into something else.
Tagmentization is the result of modifications so that some of the
somites act together as the cephalothorax, and others
from the abdomen.
Many arthropods have taste receptor sensilla on exterior mouthparts, on their legs, on their antennae, and even on their wings. These may seem like a lot of work to develop them on so many different structures, but maybe not. Metamerism is at work.

Metamerism (meta = subsequent, and mer = unit) is a biology concept for efficient addition of complexity in an animal. Over time and evolution, certain specific structures and functions may develop in response to pressures. It is much more efficient to just create another unit using the same blue prints instead of creating a new part from scratch. The repeat is metamerism; the specialization over time of the different mers is called tagmatization.

You can see metamerism and tagmentization at work in arthropods and annelids (worms) by looking for repeating units. Millipedes and centipedes are great examples. Their bodies are made from many copies of the same basic unit. In many animals, repetition of units allows for drift over time and slow changes in structure and function, even grouping of different mers together for special function (tagmatization).

Mers (or somites) in insects include appendages like legs. But over time, many of the appendages evolved into other structures, like mouthparts, antennae, and egg-laying apparatus. Some characteristics are retained, others are dropped or altered, and some new characteristics appear.

Feel like your being stared at? The left picture is good for showing
the mouthparts of a grasshopper. Every one is a remnant of an
appendage. The mostly come in pairs, one from each modified
appendage. On the right, the cartoon shows the different
mouthparts, the labrum (lr) and hypopharynx/labium (hp/lb)
have fused to form just one piece. md = mandible, mx = maxilla
In terms of taste, the appendages seem to have been a seat of gustatory receptor sensilla. When several appendages evolved into mouthparts, the taste receptors were there. When some appendages developed in antennae, the taste receptors were there. But there is still the chicken and the egg question - did taste receptors on mouthparts result from them being derived from appendages, or did taste receptors on legs and other appendages come from early appendages being used as mouthparts?

A run down of tasting anatomy is hard for insects as a whole, because different arthropods taste with different parts, but some structures are more common. Mouthparts seem to be a favorite, and that makes sense. Flies taste with their probsocises (am I making up the plural?), but they also taste with the ends of their legs. Arthropod legs come in segments, and the last segments are called the tarsi.

Flies can taste food with their tarsi just by landing on it, but the also have taste receptors higher on their legs as well. Honeybees taste primarily with their antennae, but other flying insects can actually taste things with their wings! Wing tasters include fruit flies and mosquitoes, and they are more of an exception than you might think. We talked above about how tasting with different parts isn’t so crazy, since metamerism is just the modification of similar starting parts. But wings are not modified appendages.

Wings actually evolved from abdominal gills, and most insects have either given up these early structures and those that have them don’t taste with them. It may be that taste receptors on wings developed on their own, or that taste is older than metamerism. We don’t know their function yet – you work on that one.

Drosophila is the quintessential research model. The left
cartoon shows the olfactory and gustatory receptors. Notice
how many taste receptors are around the proboscis. On the
right, the red dots show all the different places gustatory
receptors are found. Wing margins, legs, tarsi, and mouthparts
all have taste receptors.
We have introduced mosquitoes and taste when we talked about CO2 above, but they come into play again here, according to a 2010 study. They taste with wings, and this may have something to do with how we can keep mosquitoes away from us. The two main chemical deterrents to mosquitoes are DEET and citronella candles. And they work differently.

Citronellal is only smelled by mosquitoes; the active molecule triggers only olfactory receptors. But DEET triggers both olfactory and gustatory receptors, it is smelled and tasted. Both senses stimulate avoidance responses in insects, so even if a mosquito lands on you, the DEET you put on will be tasted and may keep it from biting.

So some insects taste with wings - is that as weird as it gets? Nope, some females taste with their ovipositors (ovi = egg, and posit = laying). Ovipositors are a result of metamerism, they are modified appendages. The females of many species can taste the plants or places they land to determine if they are a suitable place to lay eggs.

The ovipositors most likely have rare taste receptors, applied to only to this one specific task. For example, there are two subspecies of a particular fruit fly called a goldenrod gall fly (Eurosta solidaginis). The females look for specific plants, and then for buds of the right age in which to insert their eggs. The growing larvae then feed on the bud, and cause a tumor (gall) to form.

The ovipositor of a female wasp or fruit fly is also a modified
appendage. In the wasp on top has a rigid ovipositor that may
be used to inject eggs into a caterpillar larva. On the fruit fly
ovipositor below, you can almost see the sensillae that
contain the taste receptors.
The interesting point is that there are two different kinds of goldenrod and two different kinds of flies. One type of fly will never pick the other type of goldenrod to lay it eggs on. The slightly different plants must have slightly different tastes, and the two subspecies of flies have evolved to react favorably to only one of the two tastes.

Obviously, some insects pick their plants very carefully. Let me give you an example that really knocks this point home. Tiger moth (Grammia incorrupta) caterpillars are sometimes parasitized by flies or wasps that lay their eggs inside the wooly bear (tiger moth caterpillar). A 2009 paper shows that when this occurs, the caterpillars switch the kind of plant food they eat, opting for poisonous plants that contain pyrrolizidine alkaloids (PA).

The PA-rich food is much less nutritious than the caterpillar’s regular food, so it definitely costs the caterpillar in terms of grown and health, but the PA is toxic to the parasites. The food choice sometimes depends on the number of parasitic eggs laid in one individual caterpillar. Just one egg – a caterpillar may eat some PA-rich plant material and let its immune system do the rest of the work. But with more eggs, the woolly bear will consume PA-rich plants exclusively – hoping to kill off all the eggs. The caterpillars are self-medicating, tasting their way back to health.

Turnabout is fair play – we haven’t discussed the plants that are being eaten by all these insects. In some cases, it turns out that the plants are tasting them right back, and even tasting each others' messages.

You can see the parasitic wasp injecting eggs into the
caterpillar. When the eggs hatch, they will feed on the
caterpillar through their larval stage. Two things may
happen. The caterpillar may switch plants (based on taste)
to try and poison the parasites. Second, the plant they are on
now may have called in the wasps to kill the caterpillar using
volatile chemicals, and the toxic plant that the caterpillar
switches to may do it again.
Corn plants (maize) get munched on by caterpillars. In response, they produce chemicals to attract predators of the caterpillars. This has been known for a while. But a 2000 study showed that the plants respond to the caterpillars saliva; the maize tastes it (contact chemosensation) and starts to send out the volatile chemicals that will attract parasitic wasps looking to lay eggs in the caterpillars. A more recent study shows that the caterpillars play an even bigger role in their own demise.

The volatile chemical that maize uses comes in two forms; it’s the switch from primarily one form to the other that attracts the wasps. But even before the plant starts to produce the attractive form, the caterpillar’s saliva converts the inactive form to the attractive form. The attractive message starts about a day before the plant starts to make the attractive form. The maize molecule has evolved to make the caterpillar call the cops on itself.

What is more, plants can send taste messages to nearby plants through the dirt. In a 2011 study, researchers induced drought like conditions on one row of plants. In less than an hour, plants five rows away started to close their stomata (pores in leaves) to conserve water for an impending drought. Plants that were just as close, but planted in a different container did not prepare for drought, so the message had to be traveling through the soil. I leave it to you to decide if this is really a taste sense.
So - if you’re a raw food enthusiast, you might be being tasted back. And maybe your food is spreading the word about you to his neighbors. Next week – why do we call spicy food "hot?"

Falik O, Mordoch Y, Quansah L, Fait A, Novoplansky A (2011). Rumor Has It…: Relay Communication of Stress Cues in Plants. PLoS ONE, 6 (11)

Lee Y, Kim SH, & Montell C (2010). Avoiding DEET through insect gustatory receptors. Neuron, 67 (4), 555-61 PMID: 20797533

Singer, M., Mace, K., & Bernays, E. (2009). Self-Medication as Adaptive Plasticity: Increased Ingestion of Plant Toxins by Parasitized Caterpillars PLoS ONE, 4 (3) DOI: 10.1371/journal.pone.0004796

Allmann S, & Baldwin IT (2010). Insects betray themselves in nature to predators by rapid isomerization of green leaf volatiles. Science (New York, N.Y.), 329 (5995), 1075-8 PMID: 20798319

Kwon JY, Dahanukar A, Weiss LA, & Carlson JR (2007). The molecular basis of CO2 reception in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 104 (9), 3574-8 PMID: 17360684

For more information or classroom activities, see:

Carbon dioxide taste in insects –

Parasitic wasps –

DEET/citronella –

Plant volatile defense chemicals -