Wednesday, February 26, 2014

Strange Insect Tastes

Biology concepts – sensilla, uniporous sensilla, gustatory receptor, RNA world hypothesis

Chalcanthite (copper containing) is used in traditional
medicines, even though it is toxic. Recent study shows
it is anti-inflammatory when mixed with egg white. A
2013 study shows that after burning off the water from
chalcanthite and mixing it with egg white to eliminate
toxicity, the concoction inhibits several signaling
pathways that would otherwise stimulate
inflammation. I’m not sure you would have to taste
this mineral to know what it was.
Yukon Cornelius, you know- the prospector of Rudolph the rode-nosed reindeer fame, used to taste the end of his pick after ho tossed it into the air and it stuck in the ground. He was looking for gold, and the action implied that he could know if there was gold in the ground by how it tasted.

Don’t laugh, I’ve seen many a geologist taste a rock to get some information about it and the area from which it came. Halite is an easy one (Greek hals = salt), but other minerals have tastes as well.  

Borax is sweet and alkaline. Ulexite tastes alkaline while chalcanthite is sweet and metallic (see picture). There are others as well, just be careful that you have a clean area to taste, not one that has been exposed to overflying birds.

Believe it or not, this does have application in biology. Geologists are looking for older and older borates, like borax and ulexite, because there are hypotheses that these might have been important in stabilizing the ribose of RNA in the prebiotic RNA World. They field test samples by tasting to find borates to test for age.

But I don’t know about Mr. Cornelius using taste to find gold. Gold is famously inert, it shouldn’t have any taste at all. In fact, professional ice cream testers use gold spoons just so they won’t be influenced by anything but the product.

It’s not probable, but perhaps geologists and ice cream tasters learned from insects about taste. Arthropods are famous for finding interesting uses for taste. They taste their way to food, to find mates, and even to find appropriate places to lay eggs. But what is most exceptional is how and where they do it. Insects are our big exceptions for the day.

Insects (just one class of arthropods) are invertebrates, so they don’t have the traditional taste buds associated with mammals, fish, and birds. Instead they have taste receptors house inside gustatory sensilla. There are several types of sensilla on insect bodies, and different types can house different senses. Gustatory sensilla are usually of the trichome (or trichoid, meaning three faces) type, meaning that they look like hairs and most people call them hairs. They are not hairs because they are not made of keratin protein. They are made from chitin, the same material as the crunchy insect exoskeleton, and they are hollow.

This is a photomicrograph of an insect antenna, with
several different types of sensilla. Look closely to see
the differences. The sharper ones come in two lengths,
shorter (b) and longer (a), but they are both considered
trichome type. Others are blunter and thicker, these are
the basiconic type (c). Trichoid house touch and taste
receptors. Basiconic hold olfactory (smell) receptors.
The end of the sensilla has a single opening, a very small opening (10 nm/4 x10-7 in). Because of the single opening, it is also called a uniporous sensilla.  The pore is so small that water molecules trapped within it can’t evaporate. If the sensilla then rubs up against a surface and some surface molecules get trapped in the water. These molecules can stimulate the gustatory receptors and the insect can taste what they have touched.

These sensilla are common among the arthropods. The arthropod phylum includes the chelicerae (scorpions, spiders, etc), myriapoda (millipedes and centipedes), hexapods (insects, beetles, ants, butterflies, etc.), and crustaceans (crabs, lobsters, shrimp, etc.). I was surprised to find that crayfish and lobsters have sensilla on their legs – antennae, O.K., but on those hard legs? Spiders, even the ones that aren’t hairy, have gustatory and olfactory sensilla, as do millipedes and similar. Since there are more than 500 arthropod species for every mammalian species on Earth, it would seem that uniporous sensilla are the common way to taste. Taste buds like ours are the exception.

The gustatory receptors of arthropods are located on neurons housed within the sensilla. The neuron depolarizes based on the strength of sense signal and transmits that information to the central nervous system. We’re talking about insects here, so “brain” isn’t really the right word to use. In arthropods, both gustatory and olfactory inputs go to an olfactory center, so one could argue if it is really a taste they are sensing. It’s perceived in the smell center, but comes from direct contact, not a gaseous molecule from a distance – let the discussions begin.

However they perceive it, gustatory receptors in uniporous sensilla of insects are used for a variety of purposes. That’s not exceptional – we do too. But insects tend to do it better and for more varied reasons. The obvious function is for finding food, but here insects take shortcuts that other animals do not. Take, for instance, one of the most important research animals ever, the fruit fly (Drosophila melanogaster).

Top left: the proboscis of the fruit fly can be seen projecting
forward, like an insect elephant trunk. Top right: the
proboscis monkey, while at the bottom is the Darwin’s hawk
moth. The term “proboscis” can be used with invertebrates
or vertebrates, but it means different things in each case.
When speaking invertebrate, proboscis means tubular
mouth parts. In the vertebrate tongue, it doesn’t mean
tongue at all, it means nose or snout.
The fruit fly shortcut is seen when it tastes something sweet or tastes water, the neural circuitry automatically causes muscular movements that extend the fly’s proboscis (pro = forward, and boskein = to feed) for feeding. Similarly, if the fly tastes something bitter, the reflex is for the proboscis to retract and feeding to either stop or not start. Muscle movements are connected directly to taste sensation. We can’t do that, unless you count the face kids make when they eat broccoli.

Also in feeding, it seems that insects are the exception to the rule of a limited number of taste receptors. Insects that feed on only one type of plant (feeding specificity) tend to evolve taste receptors for chemicals made only by that particular plant. This leads to many receptors with novel and new specificities.

Depending on the diet or other uses for receptors, insect species also vary greatly in the number of different receptor genes they have. Fruit flies have more than 70 different receptor genes, while honeybees may have as few as ten. However, they probably all have a receptor for tasting water.

The water receptor was recently identified in Drosophila. A 2010 paper in Nature describes a gene and protein called pickpocket 28 (ppk28). The scientists tracked the brain responses to water in flies when the gene was stimulated or when they removed the gene.  There was more activity when plain water was given than when it was mixed with salt or sugar (more water if no solute). When mutated to become nonfunctional, flies drank water for much less time (3 seconds versus 10 seconds) and showed much less brain activity in response to water.

Studies like this are hard, but the amount of brain space devoted to sensing things like this makes it easier. Undoubtedly, the ants (still in the arthropod phylum) are king when it comes to sensing taste and smell. For example, worker ants can distinguish between different single and double sugars, meaning that they differentiate many subtle differences in taste.

Here we witness a heartwarming act from the animal world.
C. japonicus ants have adopted the fusca caterpillar out of the
goodness of their hearts. Don’t even consider that the
caterpillar has tricked the others into think he is an ant, or
that the ants feed him just so he will secrete sugars that the
ants can snack on. No way - it’s a Hallmark special, not a
reality TV episode.
But they can also select different sugars based on immediate needs; whether they would be good for stored energy or immediate energy. This suggests nutrient sensing as well as taste differentiation. For example, Camponotus japonicus ants have a symbiotic relationship with Niphanda fusca butterfly larvae (caterpillar).

The ants protect the caterpillars because the caterpillars provide the ants with sugars, specifically, a disaccharide called trehalose + an amino acid, glycine. The ants actually adopt the caterpillars and raise them with their colony because the caterpillars secrete a pheromone that mimics that of the ants. The ants accept them because they taste like one of their own. The gift of sugar reinforces the relationship.

Other ant species will select different sugars equally, but the C. japonicus ants prefer trehalose. What is more, those ants prefer trehalose + glycine even though no ant species prefers glycine alone. So in this species, symbiosis drove evolution of a taste receptor for trehalose, and is modified by glycine.

One last example on ants, leaf cutter ants (Atta vollenweideri) produce different taste receptors based on the caste they belong to (large workers, small worker, soldiers, queens). A 2013 paper shows that the different castes and subcastes also have different numbers of taste receptors on their legs and antennae, so they respond to stimuli differently. One stimulus might be cohorts (members of the same colony) or, in other insect cases, for finding mates.

Drosophila fruit flies have been studied for this as well. A 2012 paper showed that different gustatory receptors and different pheromones are found on male and female flies. Fruit flies perform many different courtship rituals, and these take energy and time. It wouldn't pay to be courting another male – so sensing whether another fly is male or female is important.

Courtship in fruit flies is more complex than teenage dating.
The motions shown above are just a few of the actions that
take place, but the others aren’t G rated, so I decided not to
show them. The male doesn’t pick the female based on looks,
smarts, or ability to stick to a budget. New research shows
that he picks her based on the fact that she doesn’t
taste like a male.
This study mutated certain taste receptors. When male receptors are stimulated by male pheromones, courtship rituals stop. But if a female is tasted, the courtship continues. In the mutant flies, males would court males. When only mutant males were placed together in a container, they would line up in a long line, one fly courting the male ahead of it and being courted by the male behind it.
In butterflies, these different receptors give clues about evolution.  In the postman butterfly (Heliconius melpomene), researchers found 73 putative gustatory receptor genes, but the number of copies of gene and the variations of some genes varied between males and females. Fully one third of the genes shows a female bias in expression level, many being found on female legs, but not male legs. The results also showed that many of these were also the result of many recent gene duplications. 
Gene duplications allow for more genetic drift, and this would result in a greater number of possible receptors. Varied expression suggests that females are using the receptors for things that the males are not. So female behaviors seem to driving the expression and evolution of the gustatory receptors in butterflies. Once again, the women are in charge.

Next week, we should look at the weird places insects have taste receptors and how taste plays a role in egg laying. Even weirder, insects may taste plants, but it turns out that the plants are tasting them right back.

Choi EA, Park HY, Yoo HS, & Choi YH (2013). Anti-inflammatory effects of egg white combined with chalcanthite in lipopolysaccharide-stimulated BV2 microglia through the inhibition of NF-κB, MAPK and PI3K/Akt signaling pathways. International journal of molecular medicine, 31 (1), 154-62 PMID: 23128312

Briscoe AD, Macias-Muñoz A, Kozak KM, Walters JR, Yuan F, Jamie GA, Martin SH, Dasmahapatra KK, Ferguson LC, Mallet J, Jacquin-Joly E, & Jiggins CD (2013). Female behaviour drives expression and evolution of gustatory receptors in butterflies. PLoS genetics, 9 (7) PMID: 23950722

Koch SI, Groh K, Vogel H, Hansson BS, Kleineidam CJ, & Grosse-Wilde E (2013). Caste-specific expression patterns of immune response and chemosensory related genes in the leaf-cutting ant, Atta vollenweideri. PloS one, 8 (11) PMID: 24260580

Thistle R, Cameron P, Ghorayshi A, Dennison L, & Scott K (2012). Contact chemoreceptors mediate male-male repulsion and male-female attraction during Drosophila courtship. Cell, 149 (5), 1140-51 PMID: 22632976

For more information or classroom activities, see:

Mineral taste –

Uniporous sensilla –

Proboscis –

Niphanda fusca

Leaf cutter ants -