The implication of the steeper angle of incline of amphioxus and vertebrate myosepta, in comparison with Pikaia, is that the forces generated by myomere contraction are a more serious issue for amphioxus and fish, requiring this adaptation, than for Pikaia. It is thus reasonable to suppose that Pikaia myomeres would not have been capable of exerting as much force as those of modern chordates, and consequently peak swimming speed in Pikaia would have been considerably less. There is an assumption here, as the conclusion depends on the supposition that angling of myosepta gives a direct measure of the force of contraction across a range of taxa, both living and long extinct. For this to be true, the angle of inclination must be a comparatively plastic feature in evolutionary terms, one that is able to adapt rapidly in any lineage when it is advantageous to do so. This may be reasonable because, as structural features go, myomere shape is one that in principle should be easy to adjust incrementally. Indeed, myomeres in nearly contemporaneous vertebrates such as Haikouichthys[12], which are roughly intermediate in shape between those of Pikaia and amphioxus, show an incremental gradation in shape along the body. Those in the caudal region are more steeply inclined, which is precisely where one would predict the greatest stress if, for example, the animals had an escape response involving powerful tail flips.
There is a further issue that needs to be considered in this context, and that is the nature of the muscle fibers themselves. Myomeres in amphioxus and fish have basically two fiber types with quite different functional capabilities [13, 14]. Rapid, episodic burst swimming results from the contraction of fast (or fast-twitch, or deep) fibers, of which the bulk of the myotome is composed. In addition, however, there are sets of slow (slow-twitch, or superficial) fibers along the lateral margin of the myomere, fibers that do not fatigue as quickly and are responsible for prolonged bouts of slower swimming. These are used for long distance swimming (for example, cruising or migration) in fishes, for diurnal vertical migrations in the water column in amphioxus larvae, and to adjust position in burrows in adult amphioxus. With regard to amphioxus specifically, there is a lingering misconception that the burrowing habit has resulted in its becoming a rather poor and ineffective swimmer. The contrary is, in fact, the case, as anyone who has tried to net an amphioxus swimming at peak speed will attest. The animal is mass of muscle and connective tissue capable of powerful writhing movements when restrained, and of considerable speed when swimming, greater than many fish when adjusted for relative body size [15]. In part this is possible because, lacking eyes, amphioxus need not look where it is going. Instead, and because of its tough cuticle, it simply bounces off obstacles in its path. Such behaviors are due to the action of the fast fibers, and are well described in previous accounts of the behavior of larvae [16, 17] and adults [18]. Clearly, a much greater physical stress is being exerted on the support structures of the body during fast than slow swimming, which must certainly be a factor in explaining the adaptive advantages of V-shaped myotomes.
The conclusion one can draw from this is, that because Pikaia lacks steeply inclined myosepta, its muscle fibers have properties more like slow fibers than fast ones. If it could be shown that the slow system evolved first, Pikaia could quite logically be interpreted as representing a stage in chordate evolution before the evolution of fast fibers. With some further biomechanical analysis of contraction strengths, septum thickness, and so on, a good deal could probably be inferred about the behavioral capabilities and mode of life of Pikaia based on the known properties of modern slow fibers. However, the evidence for a sequence in the evolution of fiber type, of slow before fast or vice versa, is at best circumstantial. Logically, one might suppose that the less effective locomotory mode would have evolved first, with subsequent improvements being a response to extraordinary new adaptive pressures. Since the Lower to Middle Cambrian was a period when fast-swimming predators with high-resolution eyes were appearing (chiefly the anomalocarids and their kin [19]), slow modes of swimming that would have been adequate for basal chordates nearer the dawn of the Cambrian would have been increasingly less so. Faster modes would have had to evolve. That this happened quickly is evident from the vertebrates of the time, for example, Haikouichthys, as mentioned above, which predates Pikaia by 5 million years at least. Conodonts, though much later, also have this feature [20, 21], as befits another putative basal vertebrate. Both belong to lineages that survived the Cambrian, whereas Pikaia evidently, so far as we know, did not.
The developmental sequence is suggestive here as well. In fish (from zebrafish data), the slow fibers develop first, and then migrate to the outer surface of the somite [22, 23]. The fast fibers develop later, but depend on cues from the slow fibers for correct deployment [24], while myoseptum formation is also impaired in the absence of slow fibers [25]. That slow fibers are so fundamentally important to the normal sequence of developmental events is certainly consistent with an early origin, possibly predating the evolution of the later developing fast fiber system, but there are other interpretations (see below). Further evidence for the relative antiquity of the slow system, again circumstantial, comes from amphioxus, where there are significant differences in the way the two systems are innervated. From data on larvae [17, 26] fast fibers are innervated by neurons distributed along the nerve cord via conventional synapses, and mechanosensory input is routed to this system alone as befits an escape pathway. The slow system, in contrast, is innervated by a dedicated series of neurons in the anterior nerve cord via a less specialized type of synaptic contact. The principle inputs, so far as this has been determined, is from neurons in the cerebral vesicle, specifically in the amphioxus homolog of the hypothalamus, and from the dorsal ocelli (eyespots). In both the hypothalamic and ocellar pathways, paracrine release from large terminals predominates over specialized synapses. The former, where it occurs (for example, in core limbic elements of the vertebrate brain), is generally considered an indication of evolutionary antiquity [27]. The involvement of the ocelli in the slow circuits may also be significant, since response to light both during vertical migration (in larvae) and in burrows (adults) are aspects of feeding behavior, and hence sufficiently basic to survival that they probably predate the rise of visual predators. In addition, because the neurotransmitter in these photoreceptors is related to a gonadotropin-releasing hormone [28], there is a possibility that the ancestral function of the slow system was in some way involved with reproduction or mating behavior.
While the above is consistent with the slow system being evolutionarily older, there is an alternative suggested by molecular data on fiber type specification: that the fast fibers are the default state of myocyte development, while the slow fibers follow a divergent pathway initiated by early Hedgehog signaling from the notochord [29]. This would imply that slow fibers, at least in their modern form, are a late addition to an older program of myocyte differentiation. However, even if the mechanism controlling fast fiber differentiation is an ancient one, it does not mean that the ancestral fibers matched modern fast fibers in their functional capabilities. Quite the converse, since on the evidence of myomere shape in Pikaia, it would seem that the forces generated by the ancestral fibers were much less, probably more like modern slow fibers than fast ones. Suppositions concerning the behavior and mode of life of Pikaia need then to be assessed with this in mind.
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