Swimming in the Cambrian

If you ever get a chance, spend some time looking at fish muscles in a microscope. Larval zebrafish are perfect; they're transparent and you can trace all the fibers, so you can see everything. The body musculature of fish is most elegantly organized into repeating blocks of muscle along the length of the animal, each segment having a chevron ("V") or "W" shape. Here's a pretty stained photo of a 30 hour old zebrafish to show what I mean; it's a little weird because this one is from an animal with experimentally messed up gene expression, all that red and green stuff, but look at the lovely blue muscle fibers stretching across the length of each segment.

Lateral view of a 30 hour old zebrafish, embryonic myotome, displaying ectopic eng2a:eGFP (green) fibers in response to Smad7 (marked in red) expressing clones. Slow muscle fibers are marked by monoclonal antibody F59 (blue).

But wait—why the chevron shape? Also, the reason I told you to look in a microscope sometime is that a 2-D image can't illustrate the lovely intricacy of the muscles; they don't go straight across, but twist in a partial spiral in 3-dimensions. Trust me, it's beautiful to see. And it's also nearly universal in chordates — even Amphioxus has this arrangement. And there's a good biomechanical reason for this arrangment.

Each of those muscle fibers is attaching to a connective tissue band in the line between each block of muscle, called a myoseptum. The force of contraction of the muscles is going to pull on these connective tissue anchor points, stressing them. By organizing all of the fibers to pull at an angle rather than perpendicularly to the myoseptum, it reduces the amount of force directly applied to the septal connections by as much as 50-60%, depending on the angle, relative to the overall force of contraction applied to generate the bending movements.

The beneficial consequences of having chevron- or V-shaped myomeres, illustrated using amphioxus. (A) The V shape guarantees that the force acting perpendicular to the myoseptum (vector P) is less than the force of contraction (vector F) by an amount that increases with increasing angle (θ) to the vertical. The degree of incline shown is typical for amphioxus larvae, and increases with increasing age. (B) Somite overlap in young adult amphioxus, modified from [11]. The central components of the locomotory system are the notochord (not, shown in violet) and the nerve cord (green). These are bound to the myomeres (pink) by sheaths of basal lamina (blue). The V-shaped myomeres are positioned so that the tip of the caudal-most in any section is adjacent to the notochord, while the extended tails of progressively more anterior myomeres (shown in progressively lighter shades, compare with A) are ranged above and below. Because every point along the notochord has essentially the same complement of septa, this arrangement ensures that the force of contraction experienced by the notochord is distributed evenly along its anteroposterior axis, rather than being borne at specific sites.

An additional benefit is that the angle distributes the force generated by a single segment's contraction to a longer stretch of the notochord, the central springy rod that forms the main axis of the skeleton.

So why do fish do this? Because with powerful muscle contractions needed for fast swimming comes the potential for tearing connective tissue and buckling or damaging the central skeleton. These are adaptations for rapid, efficient swimming. They are also necessary for escape responses: startle a fish, and it makes an abrupt, massive contraction of these muscles to flick it out of danger. That behavior wouldn't be so useful if it ended up tearing muscle insertions and crippling the fish within seconds of its escape.

Which suggests that it would be interesting to look at fish that don't have these geometric properties. That's easy, too: just look at embryos! Below is a timelapse of the segments forming one by one in an embryonic zebrafish; it's very short and zips by, so I've also got a step by step breakdown of what's going on.

The key observation is that the segments initially form with straight up-and-down boundaries. Even within one animal, though, you can see a progression: the newest-formed segments are to the right, and older ones are to the left, and you should be able to see that they start out simple lozenge-shaped blocks, but within an hour they bend in the middle to form a chevron shape.

Embryos, obviously, are very poor swimmers and can generate only feeble contractions. They get stronger as more muscle fibers differentiate and as they bend into that more efficient conformation.

The morphology informs us about the physiology and behavior. We can get a good idea of what kind of swimming fossil organisms were capable of by looking at the shape of their body parts. Here, for instance, is the Cambrian chordate Pikaia, sufficiently well preserved in the Burgess Shale that we can actually see the arrangement of its muscles. Which are not impressive.

Pikaia gracilens, as reconstructed by Conway Morris and Caron.The head bears a pair of tentacles, probably sensory in nature, and paired rows of ventrolateral projections that may be gills. Not shown: the expanded anterior (pharyngeal) region of the digestive tract, and the dorsal shield-like structure, the anterior dorsal unit, that lies above it. The boxed detail shows the main axial features: the dorsal organ (do), and the putative notochord (not) and digestive tract (dt). The size range among specimens is 1.5 to 6 cm, which makes this animal very close in size to the adult stage of modern lancelets (amphioxus).

Pikaia was definitely not a darter, but more of a slow, undulating swimmer…and it wasn't very fast at that. We can put together a reasonable picture of the Pikaian life-style.

If one assumes that Pikaia was incapable of a fast escape from visual predators of the Anomalocaris type, a strategy of avoidance would likely be its preferred solution. Pikaia was probably not, therefore, an animal that spent a lot of time high up in the water column or near the surface dur- ing daylight hours. One could envisage it feeding inconspicuously near the bottom, perhaps cruising along and browsing on benthic detritus or microbial mats, direc- ted by its paired sensory tentacles. This accords with the conclusions of CMC that, from the mode of preservation, Pikaia was likely epibenthic rather than fully pelagic. Alternatively, it may have migrated vertically to spend time feeding at the surface, but only at night. Unfortunately, as the apparently tiny mouth is difficult to interpret in the fossils, there is little direct evidence from the morphology as to how Pikaia fed. Because the mouth was not large, it seems unlikely that Pikaia took in large volumes of water when feeding, however, as a suspension feeder normally would be expected to do.

A speedier chordate of the same era would have been Haikouichthys, which does have the complex segmental morphology of an efficient swimmer. Muscle morphology tells us that there were diverse behavioral strategies being played out by early chordates even in the Cambrian.

Lacalli T (2012) The Middle Cambrian fossil Pikaia and the evolution of chordate swimming. EvoDevo 3:12.