Some of you may have never seen an arthropod embryo (or any embryo, for that matter). You’re missing something: embryos are gorgeous and dynamic and just all around wonderful, so let’s correct that lack. Here are two photographs of an insect and a spider embryo. The one on the left is a grasshopper, Schistocerca nitens at about a third of the way through development; the one on the right is Achaearanea tepidariorum. Both are lying on their backs, or dorsal side, with their legs wiggling up towards you.
There are differences in the photographic technique — one is an SEM, the other is a DAPI-stained fluorescence photograph — and the spider embryo has had yolk removed and been flattened (it’s usually curled backward to wrap around a ball of yolk), and you can probably see the expected difference in limb number, but the cool thing is that they look so much alike. The affinities in the body plans just leap out at you. (You may also notice that it doesn’t seem to resemble a certain other rendition of spider development).
True beauty is more than skin deep, though, so now I’m sure you’re all wondering what molecules mediate the specification and further development of the pattern on display in these arthropods. Sad to say, there seems to be a real dearth of research on spider development, and I’ve only found a few papers that discuss spider evo-devo. I’ll briefly summarize one, though, that has an interesting message: axis formation in spiders, flies, and vertebrates use many of the same molecules for pattern formation, but there are differences…and flies in particular seem to be highly derived (no surprise there), while both spiders and vertebrates seem to have retained some of the more primitive rules of dorsal/ventral specification, and are more similar to each other.
The general issue is one of determining how embryos set up one axis, the dorsal/ventral (back/front) polarity. One common strategy when establishing any kind of polarity is to have one ubiquitous molecule that defines one pole and then to have a second molecule that antagonizes or blocks the first set up at one place to establish a second pole. Cells in the embryo can then ‘read’ the relative levels of the two molecules to determine their position along the axis.
In early vertebrate embryos, we have one molecule that is all over the place that is called Bmp-4 (for bone morphogenetic protein 4). This molecule is a ventralizer: that is, if this were the only signal given to all of the cells in the embryo, they would all form ventral tissues — you’d have an embryo that is all belly, with no dorsal tissues like a notochord or nervous system. There are several molecules that are dorsalizers, or specify the formation of those dorsal tissues, but one of the most prominent is called chordin. Chordin antagonizes Bmp-4, clearing its ventralizing effects, and is expressed in an area called the organizer, which goes on to establish the dorsal part of the animal.
Invertebrate embryos do something very similar. They also have a molecule that is homologous to chordin, called sog (for short gastrulation), which antagonizes another molecule called dpp (short for decapentaplegic, and aren’t you glad they shortened that one?), and the interactions between these two molecules help establish the dorsal/ventral axis. Sog is expressed in the midline where the nervous tissue is located, while dpp is found on the opposite side, in an extraembryonic tissue called the amnioserosa.
There is a complication, though, that sometimes confuses people. Arthropods have a ventral nerve cord; pick up an insect, flip it over, and the nervous system is actually located along a midline seam that runs between the animal’s legs. Vertebrates have a dorsal nerve cord; pick up a mouse, and don’t flip it over — the spinal cord runs along its back. The chordin/sog molecule in the embryos of both is expressed where the nerve cord will form, so it’s a dorsalizer in mice and a ventralizer in insects, but it’s doing the same thing.
I know, the terminology messes everyone up. Someday the developmental biologists should sit down and revise the nomenclature so that the body axes are defined by domains of homologous gene expression rather than by arbitrary spatial axes, because it’s become increasingly clear that one lineage or the other (and it was probably the chordates) experienced a radical, ancient spatial inversion while retaining the common molecular coordinates.
Another complication: in flies, sog is important in antagonizing dpp, fine-tuning dpp’s expression to just a sharp strip in the amnioserosa (dorsally), but it doesn’t seem to be particularly important otherwise in establishing ventral tissues like the nerve cord and mesoderm. Those jobs have been taken over by other molecules. The business of antagonizing the dpp/Bmp signal has been shunted into a supporting role rather than being the crucial event in setting up the axis.
So two differences between chordates and flies are 1) the inversion, which we’ll ignore, since from the point of the function of the molecules it is mostly irrelevant, and 2) that flies have made dorsal/ventral axis specification rather more intricate, separating the roles of blocking the signal for the other pole from the job of actually specifying the tissues of its side of the animal. The question is, where do spiders fall in the range of roles for sog/chordin and dpp/Bmp? In particular, is spider sog like fly sog, in that its role is to simply fine-tune dpp expression, or is it like vertebrate chordin, which also has a role in establishing tissue types in the region of its expression?
This is a data-rich paper, thick with photographs of complicated patterns of gene expression of sog and dpp at different stages of development in two species of spider (Achaearanea tepidariorum and Pholcus phalangioides) and the brine shrimp, Artemia franciscana, with staining for the genes single-minded, prospero, engrailed, and optomotor blind thrown in. It’s available online if you’d like to get all the details, but I’ll gloss over it all, interesting as it is, and give you just the take-home message: the early patterning of the spider dorsal/ventral axis seems to be more like that of a chordate than a fly. The sog gene product does play a more active role in specifying the tissues along the d/v axis.
Just one example of the data: they used dsRNA to knock out expression of sog in the spider embryo, and what was observed was a range of destruction of ventral midline structures. The most dramatic phenotype was that the limb buds fused along the midline, making the strangely wormlike creatures seen in A, below.
Wait, wait … spiders more like chordates than they are flies? Doesn’t this violate evolutionary expectations? I can just imagine the creationists getting excited about this — but they’d be wrong, for a couple of reasons.
One is that despite being in the same arthropod clade, arachnids and insects have diverged for a very long time, with all of the divergences between arachnids and insects and arthropods and chordates occurring before the Cambrian. What we’re seeing is that there was a primitive mechanism for axis specification that all of these lineages shared initially, and that two of them have retained aspects of that early mechanism, while one, the insects (or at least, the flies) have diverged significantly.
Just generally, flies are unusual, specialized and rather highly derived animals. We’re constantly running into this issue that the standard animal for molecular genetics work for many years is turning out to be a peculiar oddball in many ways. We study the little two-winged freak and lose perspective a little bit — when we start comparing it to other organisms, we initially think they are a little weird, but we’re seeing more often now, as in this example, other critters have shared features that make them more representative of the ancestral condition.
However, we also have to be careful of that interpretation. We also know far more detail about fly development and genetics, and it’s the little differences in other organisms that jump out at us. Some of the similarities in the developmental circuitry of spiders and chordates are going to be a consequence of our sketchier knowledge about both — give the research more time, and as we gather more information about both we’ll find more and more differences. All species are going to be unique — as the depth of our knowledge about them increases, it’s easy to focus on their differences rather than their similarities.
Akiyama-Oda Y, Oda H (2006) Axis specification in the spider embryo: dpp is required for radial-to-axial symmetry transformation and sog for ventral patterning. Development 133:2347-2357.