I work with maggots. Not big fat maggots you use for fishing, but Drosophila maggots. They are incredibly simple, but are capable of performing most of the behaviours shown by the adult fly (with the obvious exceptions of mating and flying). The tiny fly Drosophila was chosen by Thomas Hunt Morgan at the beginning of the last century when he decided to study evolution. After a few years, his attempt to make Drosophila evolve was coming to nothing, when he found a white-eyed mutant fly. The rest, as they say, is history, as Morgan and his students revealed the laws of genetics that had been sketched out half a century earlier by Mendel.
Throughout the 20th century, Drosophila was studied by geneticists, and it was the first multicellular organism to have its genome sequenced, just as the new millenium dawned. Now there are hundreds of laboratories around the world studying the genetics and neurobiology of Drosophila. It would be fair enough to imagine that we knew almost everything there is to know about which cells do what in the fly, and even more so in its juvenile, more simple form, the maggot. How wrong that would be!
An article soon to be published by Nature from the world-famous laboratory of Lily and Yuh Jan describes the astonishing finding that Drosophila maggots – and, you can be pretty sure, virtually every other kind of fly maggot – is covered with tiny “eyes”. Nobody had any idea that this was the case.
Up until today, the maggot’s “eyes” were thought to be a group of 12 cells called Bolwig’s organ. They are named after the Danish scientist Niels Bolwig, who did his doctoral thesis on vision in fly maggots, and later went on to pioneer studies of primates in the wild; he died in 2004. There are two Bolwig’s organs, which you might imagine are the dome-shaped things on the front of the maggot’s face below. These structures are in fact the maggot’s “nose” or dorsal organ (my favourite bit of a maggot).
Bolwig’s organs, as shown in this lovely image by Bala Iyengar, are not at the front of the face, but instead deep inside the maggot’s body:
The Jan lab show that if the Bolwig’s organs are killed, maggots would still avoid light – (b) below – just like normal maggots (a) below:
There’s a great video on the Nature website showing a Bolwig-less maggot squiggling away from the light.
This proves that there must be some other cells in the maggot that can detect light (there was no change in temperature when the maggots had a light shone on them). Furthermore, Bolwig-less maggots did not respond to green or red light, but did avoid short-wavelength light at high intensities.
The paper reports that a particular set of cells in the maggot’s body wall, called class IV dendritic arborization neurons, responded to light – even when they were grown, isolated, in culture. These cells cover the whole of the maggot, as seen in this dramatic image – all the green cells are class IV neurons, and every one is an “eye”!
Amazingly, it turns out that these cells also express a taste receptor, Gr28b, which may be directly involved in sensing light, although this has yet to be demonstrated. This isn’t quite so surprising in that in the nematode worm C. elegans, a similar gene is also involved in responses to light. Another protein, TrpA1, which is involved in responses to light in the adult fly, is necessary for these class IV neurons to respond.
The authors conclude:
Our study has uncovered unexpected light-sensing machinery, which could be critical for foraging larvae to avoid harmful sunlight, desiccation and predation. By providing precedence for photoreceptors strategically placed away from the eyes, our finding of an array of class IV dendritic arborization neurons with elaborate dendrites tiling the entire body wall, and acting as light-sensing antennae, raises the question of whether other animals with eyes might also possess extra-ocular photoreceptors for more thorough light detection and behavioural response.
Even more importantly, this surprising result shows quite how much we have yet to discover about this animal about which, many people might have thought, we knew virtually everything. We know so much, but so little!
Yang Xiang, Quan Yuan, Nina Vogt, Loren L. Looger, Lily Yeh Jan & Yuh Nung Jan (2010). Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall. Nature. doi:10.1038/nature09576