On the origin of limbs

The evolution of animal limbs is a subject that has perplexed palaeontologists for a long time. Fossilisation is a very rare occurrence - less than 0.1% of all species ever to have lived have become fossilised, and so finding missing links in evolutionary biology is very difficult. This was the case for the origins of limb development, until very recently. Galeaspida are an extinct group of jawless fish, dating back as far as 430 million years ago. But, until recently, only their heads have ever been preserved. I spoke with Phil Donoghue, from the University of Bristol, about this new galeaspid discovery, which sheds light on the moment that these early fish developed the paired fins that may have led to our own arms and legs.

Phil - The real frustration, despite having tens of thousands of these fossils, is that all we've had until now are their heads. And the discovery that we've made now is a series of specimens of galeaspids, which preserve the rest of the body, providing us with insights into how the rest of the body plan of jawed vertebrates evolved.

Will - From what I've seen of it, it is a striking looking specimen, this fossil. But for the benefit of our audio listeners, what does it look like?

Phil - Well, it's a beautiful fossil, but beauty is in the eye of the beholder. It's basically a dead fish, and it's preserved at least as we see it, with the bottom of the body facing upwards. And it's fairly squashed. But the amazing thing is that it has a series of paired fins that extend vertically, almost entirely three dimensionally extending up from the body. It's the kind of preservation you never see in fossils of this type. And these fins extend all the way from the back of the head all the way to the tip of the tail in a way that we don't see in any living vertebrate and indeed any fossil vertebrate until now.

Will - And how did you come about this fossil?

Phil - Luckily, I had a graduate student about a decade ago with whom I started working on galeaspids. He's since gone back to China, and he and his colleagues made these amazing discoveries and were generous enough to invite me and to help describe them and interpret them.

Will - When you saw this, what gave it away to you that this fossil, this galeaspid, was the one that you were looking for?

Phil - Well, it was easy, really. It wasn't just a head. There was another three quarters of a body extending from the back of the head. And it had anatomical features, which we really didn't know that galeaspids possessed. And the key thing are these fins, really. All jawed vertebrates have a pair, unless they've lost them, a pair of anterior appendages, whether they're fins or whether they're limbs, and a pair of posterior appendages, again whether they're fins or whether they're limbs like our legs, and they're set entirely separate from each other. But in this galeaspid, which is probably the first vertebra to have paired appendages, they extend all the way, as I say, from the back of the skull all the way through to the tip of the tail. And what this suggests is that this is the precondition from which separate fins and limbs ultimately evolved.

Will - And whilst this might sound like a bit of an obvious question, why do you think they evolved the first limbs? What was the evolutionary advantage to it?

Phil - Well, the evolutionary advantage seems to have been if you extend from a cylindrical body, if you extend paired structures out, they appear to just generate lift. They allow you to effectively swim without putting any energy into the system whatsoever. It's just a product of the geometry of your body. The fins that these organisms possess weren't muscular. They couldn't move in any way, like the fins of all living, vertebrates and limbs,of all living vertebrates. That's a phenomenon that evolved seemingly much later in vertebrate evolution. But nevertheless, it's this precondition, this is adaptive benefit of being able to locomote without expending any energy seems to be the reason for why paired appendages first evolved.

Will - And how does this discovery change our preconceived timeline of appendage development?

Phil - So previously, again, based on fossils, if you set aside our new evidence from galeaspids, it seems quite clear that a more advanced group called the osteostraci, they just have seemingly just paired equivalent of our arms. So a pair of anterior fins. And these were flexible and these were muscular. And so we don't really see the equivalent of pelvic appendages, the equivalents of our legs until the origin of jawed vertebrates. So all of the evidence coming from developmental biology trying to understand the developmental basis of how fins and limbs have evolved, has been interpreted within this framework from the fossil record, suggesting that pectoral fins evolved first and pelvics evolved later. But the evidence from galeaspids suggests that actually, no, that's not the case. These are just peculiar conditions of derived osteostraci, for instance. And the condition in galeaspids suggest that the primitive state in which is one in which you have continuous fins extending from a pectoral through the pelvic position all the way to the tip of the tail. And it's actually the separation of that continuous zone of competence for developing fins that the differentiated anterior and posterior paired fins ultimately evolved.