Thursday, October 20, 2005

Getting a head in the world...

The power of segmentation has always fascinated me. Starting with some generic animal where every segment is identical, you can evolve a myriad assortment of specializations: segments with legs, with wings, with cutting jaws, with specialized hairs for digging, with paddles for swimming, flaps for moving water through a burrow, tentacles for filter feeding.... the possibilities are tremendous. The diversity that can emerge from a simple body plan through specialization of segments can be seen all around us - from centipedes and spiders to giant Atlas moths, dragonflies, lobsters and barnacles.

One of the side effects of segmentation in arthropods is their decentralized nervous system. Each segment has its own mini-brain – a cluster of neurons organized into a mass called a ganglion – that takes care of local tasks such as moving that segments appendages and collecting information from that segments sensory neurons. The arth
ropods actual brain is more of a coordinator… it tells the segment what to do, but leaves it up to that segment to handle how to do it. That’s why when you remove the head of a cockroach, the body can scuttle away in one direction while the head flops about in the other.

Interestingly, the brain of arthropods started out as a set of segmental ganglia like those found in other segments. While most segmental ganglia specialized to coordinate movement, the ganglia of the first three segments of the ancestral arthropod developed around collecting and processing sensory information, and coordinating activity for the other body segments. Even though arthropods no longer have obvious head segmentation, we can see remnants of this ancestral segmentation by looking at what appendages are directly controlled by the brain.

The arthropod brain consists of three parts – the protocerebrum at the front, deutocerebrum in the middle, and the tritocerebrum at the rear. In insects, the deutocerebrum supplies nerves to the antenna while the tritocerebrum sends nerves into the labrum (a plate in front of the mouth that helps hold food in during chewing). In crustaceans, the deutocerebrum and tritocerebrum feed nerves into the primary and secondary antenna respectively. In spiders, it is the deutocerebrum that handles the head appendages (in this case, the chelicerae – the ‘fangs’ of the spider).

The big question has always been where did the protocerebrum come from? Unlike the other brain segments, there are no appendages associated with the protocerebrum – instead, it sends nerves into the eyes. This has led some people to think that the protocerebrum is a special structure originating from a hypothetical anterior region called an acron that never had appendages.

However, a recent paper in Nature describes how an obscure group of arthropods known as sea spiders or pycnogonids uses its protocerebrum to control its feeding arms (known as chelifores). These animals start out almost as little body-less heads… they have only a set of chelifores and two pairs of legs, innervated by the proto, deuto, and tritocerebral ganglion respectively. As they get older, they metamorphose into a creature that resembles a very thin spider, with 4 to 6 pairs of true legs. The head retains the chelifores and the larval legs are modified into feeding appendages (palps).

a, The three appendages of the protonymphon larva (shown) correspond to the cephalic appendages of the adult pycnogonid. b, The adult male cares for embryos until hatching (Nymphon rubrum).

Neuroanatomy of sea spiders implies an appendicular origin of the protocerebral segment
Amy Maxmen, William E. Browne, Mark Q. Martindale and Gonzalo Giribet
Nature 437, 1144-1148 (20 October 2005)

While insights into the brains of arthropods are interesting in their own right, whats fascinating about these findings is that we may be getting a glimpse into the ancestral arthropod ground plan. An accumulating body of evidence suggests that sea spiders represent the earliest branch of the arthropod lineage, before it diverged into insects, spiders, and crustaceans. While sea spiders are clearly specialized and have a fossil record that only goes back to the Devonian, the presence of appendages at the very anterior of the animal is tantalizingly similar to structures found on several Cambrian fossil animals such as Anomalocaris.

Its possible that the ancestral arthropods started life much as sea spiders do – as a body-less ‘head’ with a pair of anterior feeding appendages and two pairs of legs, and that as they grew they added additional leg bearing segments. Over the course of evolution, the legs (both the original two pairs and those occurring on later segments) specialized, with the anterior legs becoming additional feeding appendages and the posterior legs devoted entirely to walking. Finally, a point was reached where the appendages of the first segment were no longer needed and they were lost in the ancestor to most modern arthropods… except for the sea spiders, which had already diverged. During the course of these events, the original three ganglia expanded their function form simply moving the appendages to coordinating the sensory input and behavior of the entire animal.

Of course, this last bit is speculation… the Cambrian fossils have left no trace of their nervous systems and little is known about the larval stages of most Cambrian animals…. but if correct, it would go a long way to explaining how simple segmentation led to the most diverse group of animals on this planet.