Lacalli EvoDevo 2012, 3:12

http://www.evodevojournal.com/content/3/1/12

COMMENTARY Open Access

The Middle Cambrian fossil Pikaia and the

evolution of chordate swimming
Thurston Lacalli*

Abstract
Conway Morris and Caron (2012) have recently published an account of virtually all the available information on Pikaia
gracilens, a well-known Cambrian fossil and supposed basal chordate, and propose on this basis some new ideas about
Pikaia’s anatomy and evolutionary significance. Chief among its chordate-like features are the putative myomeres, a
regular series of vertical bands that extends the length of the body. These differ from the myomeres of living chordates
in that boundaries between them (the myosepta) are gently curved, with minimal overlap, whereas amphioxus and
vertebrates have strongly overlapping V- and W-shaped myomeres. The implication, on biomechanical grounds, is that
myomeres in Pikaia exerted much less tension on the myosepta, so the animal would have been incapable of
swimming as rapidly as living chordates operating in the fast-twitch mode used for escape and attack. Pikaia either
lacked the fast-twitch fibers necessary for such speeds, having instead only slow-twitch fibers, or it had an ancestral
fiber type with functional capabilities more like modern slow fibers than fast ones. The first option is supported by the
sequence of development in zebrafish, where both myoseptum formation and fast fiber deployment show a
dependence on slow fibers, which develop first. For Pikaia, the absence of fast fibers has both behavioral and
anatomical implications, which are discussed. Among the latter is the possibility that a notochord may not have been
needed as a primary stiffening device if other structures (for example, the dorsal organ) could perform that role.
Keywords: Pikaia, Basal chordates, Myomere and notochord evolution, Amphioxus, Swimming mechanics, Vertebrate
muscle fibers, Yunnanozoans

Background muscles, and the authors identify an axial trace that

Zoology texts typically list four diagnostic features of could be either a notochord or a notochord and nerve
chordates: pharyngeal (that is, gill) slits or pores, a noto- cord combined. In addition, however, there are peculiar
chord, a dorsal nerve cord and serial (or segmental) features not known from living chordates: a sausage-
muscles. This last feature, represented by the somite- shaped dorsal organ running the length of the trunk,
derived myomere series in the case of cephalochordates and an anterior shield-like structure, the anterior dorsal
(amphioxus) and vertebrates, is the subject of this ac- unit, covering the head region. Pikaia does not, there-
count, stimulated by the recent description [1] by Simon fore, fit entirely comfortably with modern chordates,
Conway Morris and Jean-Bernard Caron (here referred suggesting that it is either divergent, if it is a chordate,
to as CMC) of the Middle Cambrian fossil Pikaia graci- or is a basal member of the chordate lineage differing in
lens (Figure 1) from the Burgess Shale of British significant ways from surviving members of that lineage.
Columbia. The authors interpret Pikaia as a basal Of the chordate features listed above, the first, the
chordate and, though this conclusion is provisional, it pharyngeal slits, have an evolutionary history that prob-
would be perverse to deny the key similarities between ably predates chordates by a considerable interval, be-
this animal and what would be expected of a basal cause apparently homologous structures occur in more
chordate: much of the body is occupied by a series of basal deuterostome phyla, in living hemichordates and
vertical bands resembling the septa between segmental fossil echinoderms [2-4]. Pharyngeal pores or slits, where
they occur, are assumed to play an ancestral role in
Correspondence: lacalli@uvic.ca deposit- or filter-feeding as a means for disposing of ex-
Biology Department, University of Victoria, Cunningham Building, Victoria, cess water entering the mouth and pharynx with food
BC V8W-3N5, Canada

© 2012 Lacalli; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly cited.
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overlap between adjacent myomeres nowhere exceeds more

than about one segment. CMC discuss this in relation to
the much more angled V- and W-shaped myomeres of
amphioxus and vertebrates, but there is more to be drawn
from this comparison in my view. Tunicate larvae are omit-
ted from both CMC and this account because, based on
current phylogenies [6], both they and their tail muscula-
ture are reduced secondarily to a degree that makes them
uninformative regarding the nature of ancestral myomeres.
Vertebrates, as one would expect, have the most compli-
cated segmental architecture. Myomeres in adult fishes are
substantial masses of tissue whose thickness seriously com-
plicates the task of analyzing the internal stresses generated
during swimming. This is chiefly because the tension
Figure 1 Pikaia gracilens, as reconstructed by Conway Morris
and Caron [1].The head bears a pair of tentacles, probably sensory exerted on the spinal axis as a given fiber contracts varies
in nature, and paired rows of ventrolateral projections that may be with the distance that fiber lies from the central axis. To
gills. Not shown: the expanded anterior (pharyngeal) region of the avoid producing unequal stresses across the myomere, the
digestive tract, and the dorsal shield-like structure, the anterior fibers are arranged helically and the myosepta have a com-
dorsal unit, that lies above it. The boxed detail shows the main axial
plex three-dimensional shape approximating a W [7,8]. The
features: the dorsal organ (do), and the putative notochord (not)
and digestive tract (dt). The size range among specimens is 1.5 to accepted explanation, which requires some fairly sophisti-
6 cm, which makes this animal very close in size to the adult stage cated modeling [9], is that this arrangement minimizes the
of modern lancelets (amphioxus). difference in tension experienced on the opposing faces of
each myoseptum as a means of reducing energy loss.
Myomeres in larval fish and in amphioxus are chevron-
particles. The remaining three features mentioned above, or V-shaped and are much less massive. They are flattened
which together constitute the axial complex, are respon- mediolaterally and so, in effect, can be treated as a first ap-
sible for undulatory swimming. These are considered to proximation as flat, two-dimensional structures. This
be restricted to chordates alone, and form a suite of makes it much easier to understand the biomechanical
characters that are closely linked anatomically, and that issues involved without resorting to a detailed mathemat-
operate functionally as a unit [4]. Of the three, only the ical and computer analysis. Muscle fibers in amphioxus at-
notochord has a plausible counterpart, the enteropneust tach to the myosepta directly [10] rather than to the
stomochord, in more basal deuterostomes, but the two notochord sheath, so the greatest stresses on the noto-
structures are not currently considered to be homolo- chord are borne where the septa join the sheath. But the
gous [5]. We thus have very little evidence from com- whole complex is also bound tightly together by sheets of
parative studies to indicate how the axial complex basal lamina, and therefore acts as a single unit, as
evolved, all at once or step by step, and if the latter, what opposed to relying on an array of subsidiary tendons and
the key steps might have been. CMC have made a start, bony struts to distribute the forces, as in fish. So, using
in their paper, by discussing the role the dorsal organ amphioxus as a model, what are the advantages of having
may play in antagonizing the force of muscle contraction V-shaped myosepta rather than vertical ones? The key
during swimming, at a stage in chordate evolution when seems to be in the angle of inclination, that is, the steep-
the notochord might not yet have fully taken over this ness of the V. Because the muscle fibers are aligned hori-
function. This commentary on their paper is an attempt zontally, along the body axis, it is in that direction that
to carry the argument somewhat further, using simple force is exerted during contraction. Expressed as vectors
biomechanical principles to clarify the relation between (Figure 2A), this force has two components, one directed
myomere morphology and swimming mode, and to dis- perpendicular to the anterior surface of the myomere (P
cuss some of the implications this has for the behavior in the figure), the other parallel to it (along the dashed
and mode of life of Pikaia and its kin. line). The former is the more important component, as
stresses in that direction are the ones most likely to result
Myomere shape and its implications in mechanical failure of the septa, for example, by tearing
CMC discuss myomere shape at some length because of the myomeres apart, whereas forces acting parallel to the
significant ways this differs between Pikaia and modern septa would only be important if damage by shear were
chordates. Myomeres in Pikaia are taller and narrow (box, the key issue. From simple trigonometry, the perpendicu-
Figure 1), while the myosepta, which form the interface be- lar component of force is less than the total force of con-
tween them, are gently curved, or sigmoidal, such that the traction in proportion to the cosine of the angle the
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septa attaching to it (Figure 2B). This evens out the stress

due to contraction. In amphioxus, the overlap ranges from
one to two segments in larvae to three to four in the adult,
considerably more in the latter than in Pikaia for an animal
of approximately similar size.

Multiple locomotory modes and escape from

predators
The implication of the steeper angle of incline of amphi-
oxus and vertebrate myosepta, in comparison with Pikaia,
is that the forces generated by myomere contraction are a
Figure 2 The beneficial consequences of having chevron- or more serious issue for amphioxus and fish, requiring this
V-shaped myomeres, illustrated using amphioxus. (A) The V
adaptation, than for Pikaia. It is thus reasonable to suppose
shape guarantees that the force acting perpendicular to the
myoseptum (vector P) is less than the force of contraction (vector F) that Pikaia myomeres would not have been capable of
by an amount that increases with increasing angle (Θ) to the exerting as much force as those of modern chordates, and
vertical. The degree of incline shown is typical for amphioxus larvae, consequently peak swimming speed in Pikaia would have
and increases with increasing age. (B) Somite overlap in young adult been considerably less. There is an assumption here, as the
amphioxus, modified from [11]. The central components of the
conclusion depends on the supposition that angling of
locomotory system are the notochord (not, shown in violet) and the
nerve cord (green). These are bound to the myomeres (pink) by myosepta gives a direct measure of the force of contraction
sheaths of basal lamina (blue). The V-shaped myomeres are across a range of taxa, both living and long extinct. For this
positioned so that the tip of the caudal-most in any section is to be true, the angle of inclination must be a comparatively
adjacent to the notochord, while the extended tails of progressively plastic feature in evolutionary terms, one that is able to
more anterior myomeres (shown in progressively lighter shades,
adapt rapidly in any lineage when it is advantageous to do
compare with A) are ranged above and below. Because every point
along the notochord has essentially the same complement of septa, so. This may be reasonable because, as structural features
this arrangement ensures that the force of contraction experienced go, myomere shape is one that in principle should be easy
by the notochord is distributed evenly along its anteroposterior axis, to adjust incrementally. Indeed, myomeres in nearly con-
rather than being borne at specific sites. temporaneous vertebrates such as Haikouichthys [12],
which are roughly intermediate in shape between those of
myoseptum makes with the vertical: for given force of Pikaia and amphioxus, show an incremental gradation in
contraction, increasing this angle (Θ in the figure) shape along the body. Those in the caudal region are more
decreases the stresses on the myoseptum. For amphioxus, steeply inclined, which is precisely where one would predict
from my own material and published photos [11], the the greatest stress if, for example, the animals had an escape
measured incline is in the range of 40 to 55° in larvae, de- response involving powerful tail flips.
pending on stage, and 64 to 68° for adults. This translates There is a further issue that needs to be considered in
into a reduction of force by roughly 24 to 43% in larvae this context, and that is the nature of the muscle fibers
and 56 to 62% in adults. This is a significant benefit if, in themselves. Myomeres in amphioxus and fish have basically
consequence, less is required by way of reinforcement to two fiber types with quite different functional capabilities
the enclosing system of sheath and septa. [13,14]. Rapid, episodic burst swimming results from the
There is another advantage in arranging for the boundar- contraction of fast (or fast-twitch, or deep) fibers, of which
ies between myomeres to be steeply inclined: it maximizes the bulk of the myotome is composed. In addition, how-
the overlap between myomeres and so distributes the force ever, there are sets of slow (slow-twitch, or superficial)
of contraction more evenly along the length of the noto- fibers along the lateral margin of the myomere, fibers that
chord. To illustrate this, consider an alternative, of straight do not fatigue as quickly and are responsible for prolonged
myosepta transversely oriented more or less vertically, as in bouts of slower swimming. These are used for long distance
Pikaia. If the muscles in such an animal attach only at the swimming (for example, cruising or migration) in fishes, for
septa (as they do in amphioxus), all the force of contraction diurnal vertical migrations in the water column in amphi-
would be borne at the sites where these join the notochord oxus larvae, and to adjust position in burrows in adult
sheath. Along the sheath, therefore, sites of maximum and amphioxus. With regard to amphioxus specifically, there is
minimum stress would alternate, so there is both a greater a lingering misconception that the burrowing habit has
risk of catastrophic failure (for example, by kinking) and resulted in its becoming a rather poor and ineffective swim-
less likelihood that the structure as a whole will flex mer. The contrary is, in fact, the case, as anyone who has
smoothly. In contrast, when septa are inclined to allow for tried to net an amphioxus swimming at peak speed will at-
multiple overlaps, every point along the notochord bears test. The animal is mass of muscle and connective tissue
essentially the same load as measured by the number of capable of powerful writhing movements when restrained,
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and of considerable speed when swimming, greater than are significant differences in the way the two systems are
many fish when adjusted for relative body size [15]. In part innervated. From data on larvae [17,26] fast fibers are
this is possible because, lacking eyes, amphioxus need not innervated by neurons distributed along the nerve cord
look where it is going. Instead, and because of its tough cu- via conventional synapses, and mechanosensory input is
ticle, it simply bounces off obstacles in its path. Such beha- routed to this system alone as befits an escape pathway.
viors are due to the action of the fast fibers, and are well The slow system, in contrast, is innervated by a dedicated
described in previous accounts of the behavior of larvae series of neurons in the anterior nerve cord via a less spe-
[16,17] and adults [18]. Clearly, a much greater physical cialized type of synaptic contact. The principle inputs, so
stress is being exerted on the support structures of the body far as this has been determined, is from neurons in the
during fast than slow swimming, which must certainly be a cerebral vesicle, specifically in the amphioxus homolog of
factor in explaining the adaptive advantages of V-shaped the hypothalamus, and from the dorsal ocelli (eyespots).
myotomes. In both the hypothalamic and ocellar pathways, paracrine
The conclusion one can draw from this is, that because release from large terminals predominates over specialized
Pikaia lacks steeply inclined myosepta, its muscle fibers synapses. The former, where it occurs (for example, in
have properties more like slow fibers than fast ones. If it core limbic elements of the vertebrate brain), is generally
could be shown that the slow system evolved first, Pikaia considered an indication of evolutionary antiquity [27].
could quite logically be interpreted as representing a stage The involvement of the ocelli in the slow circuits may also
in chordate evolution before the evolution of fast fibers. be significant, since response to light both during vertical
With some further biomechanical analysis of contraction migration (in larvae) and in burrows (adults) are aspects
strengths, septum thickness, and so on, a good deal could of feeding behavior, and hence sufficiently basic to survival
probably be inferred about the behavioral capabilities and that they probably predate the rise of visual predators. In
mode of life of Pikaia based on the known properties of addition, because the neurotransmitter in these photore-
modern slow fibers. However, the evidence for a sequence ceptors is related to a gonadotropin-releasing hormone
in the evolution of fiber type, of slow before fast or vice [28], there is a possibility that the ancestral function of the
versa, is at best circumstantial. Logically, one might suppose slow system was in some way involved with reproduction
that the less effective locomotory mode would have evolved or mating behavior.
first, with subsequent improvements being a response to While the above is consistent with the slow system
extraordinary new adaptive pressures. Since the Lower to being evolutionarily older, there is an alternative sug-
Middle Cambrian was a period when fast-swimming preda- gested by molecular data on fiber type specification: that
tors with high-resolution eyes were appearing (chiefly the the fast fibers are the default state of myocyte develop-
anomalocarids and their kin [19]), slow modes of swim- ment, while the slow fibers follow a divergent pathway
ming that would have been adequate for basal chordates initiated by early Hedgehog signaling from the noto-
nearer the dawn of the Cambrian would have been increas- chord [29]. This would imply that slow fibers, at least in
ingly less so. Faster modes would have had to evolve. That their modern form, are a late addition to an older pro-
this happened quickly is evident from the vertebrates of the gram of myocyte differentiation. However, even if the
time, for example, Haikouichthys, as mentioned above, mechanism controlling fast fiber differentiation is an an-
which predates Pikaia by 5 million years at least. cient one, it does not mean that the ancestral fibers
Conodonts, though much later, also have this feature matched modern fast fibers in their functional cap-
[20,21], as befits another putative basal vertebrate. abilities. Quite the converse, since on the evidence
Both belong to lineages that survived the Cambrian, of myomere shape in Pikaia, it would seem that the
whereas Pikaia evidently, so far as we know, did not. forces generated by the ancestral fibers were much
The developmental sequence is suggestive here as well. less, probably more like modern slow fibers than fast
In fish (from zebrafish data), the slow fibers develop first, ones. Suppositions concerning the behavior and
and then migrate to the outer surface of the somite mode of life of Pikaia need then to be assessed with
[22,23]. The fast fibers develop later, but depend on cues this in mind.
from the slow fibers for correct deployment [24], while
myoseptum formation is also impaired in the absence of General anatomy and mode of life: some
slow fibers [25]. That slow fibers are so fundamentally im- conjectures
portant to the normal sequence of developmental events If one assumes that Pikaia was incapable of a fast escape
is certainly consistent with an early origin, possibly predat- from visual predators of the Anomalocaris type, a strategy
ing the evolution of the later developing fast fiber system, of avoidance would likely be its preferred solution. Pikaia
but there are other interpretations (see below). Further was probably not, therefore, an animal that spent a lot of
evidence for the relative antiquity of the slow system, time high up in the water column or near the surface dur-
again circumstantial, comes from amphioxus, where there ing daylight hours. One could envisage it feeding
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inconspicuously near the bottom, perhaps cruising along played this role either alone or in concert with a noto-
and browsing on benthic detritus or microbial mats, direc- chord. The dorsal organ is the relevant axial structure
ted by its paired sensory tentacles. This accords with the here, as it may have been some kind of turgid sac or rod.
conclusions of CMC that, from the mode of preservation, Viewed from the perspective of modern chordates, few
Pikaia was likely epibenthic rather than fully pelagic. Al- zoologists would accept, given its extreme dorsal loca-
ternatively, it may have migrated vertically to spend time tion, that such a structure would be an effective device
feeding at the surface, but only at night. Unfortunately, as for attaching myomeres and antagonizing their contrac-
the apparently tiny mouth is difficult to interpret in the tion. As CMC point out, however, and discuss at some
fossils, there is little direct evidence from the morphology length, a truly basal chordate might well have had a
as to how Pikaia fed. Because the mouth was not large, it provisional and less efficient support system prior to the
seems unlikely that Pikaia took in large volumes of water evolving one dependent on the notochord alone. The
when feeding, however, as a suspension feeder normally dorsal organ could have been adequate for this purpose.
would be expected to do. Myomeres would attach along the sides of the dorsal
The series of paired appendages projecting from the organ and extend ventrally from it, probably attached to
pharyngeal region may be gills, and there are indications a midsagittal sheet (or sheets) of connective tissue.
in some specimens of small pores at their bases. The pres- Waves of contraction passing along the body would have
ence of projecting external gills rather than slits would least amplitude at the level of the dorsal organ, and be-
imply that the oxygen demand of even slow swimming come progressively more pronounced ventrally as dis-
required them. This is perhaps surprising given the flat- tance from the dorsal organ increased. The undulations
tened cross-sectional profile of the body, as it has consid- produced would thus be graded along the dorsoventral
erable surface area for respiration across the skin alone. axis, from shallow dorsally to deeper ventrally. A noto-
This is evidently sufficient for amphioxus, where gas ex- chord could add accessory stiffening at roughly the level
change is predominantly across the general surface of the of the gut, which may explain why it derives embryo-
body [30]. A need to expand the gas exchange surface fur- logically from the same rudiment as the latter. Indeed,
ther in Pikaia could be an indication that it experienced as locomotory capabilities of early chordates improved,
severe anoxia, at least periodically, due to its habitat. there might have been an increasing need for such a stif-
There is a further problem in the putative gills being fening device to damp undulations that would otherwise
located so far from the bulk of the trunk musculature. An impair the movement of the products of digestion along
extensive vascular system would then be needed to dis- the digestive tract. A notochord that evolved initially for
tribute oxygenated blood to the trunk, so vascular traces this purpose would be well placed to later take on a
should be expected in suitably preserved material. CMC more central role in body support as the need arose.
in fact identify one such trace, of what may be a ventral As CMC also point out, having the dorsal organ act in
blood vessel, but this begs the question of why there are this fashion links Pikaia to another group of puzzling fos-
no indications of vessels needed to complete the circuit. sils of Cambrian age, the yunnanozoans. These are consid-
On comparative anatomical grounds, these should lie ered by many to be chordates or close to them [31,32],
above the alimentary canal in a situation comparable to but there are other possibilities [33-35]. Yunnanozoans
the chordate dorsal aorta. have a dorsal sail-like structure that is apparently cuticu-
The notochord and nerve cord, expected as parallel larized and at least partially articulated. Muscle fibers have
axial traces, pose a different problem, because there is been reported in association with this structure [31],
no a priori reason to suppose that they should have the though this interpretation is contentious, but the very fact
same close linkage with the muscles as in modern chor- of articulation implies an ability to flex due to the action
dates. Undulatory swimming is accomplished without a of underlying muscles. Assuming this is a valid interpret-
notochord in diverse taxa, ranging from small (fluke cer- ation, yunnanozoans provide a second example of axial
cariae) to large (segmented annelids, for example, Nereis, support in a putative chordate by a dorsal structure that is
some species of which attain lengths of more than a not a notochord. With a second structure available to
meter). In chordates, the notochord acts as a compres- share the load, the ancestral notochord would have been
sion strut, resisting the force of contraction during freed of at least some of the constraints that determine its
swimming. The need for this would be especially acute size, robustness and location in modern forms. The fossils
during rapid escape swimming, but much less so for an need to be interpreted with this in mind.
animal capable only of slow swimming. This is not to
say that Pikaia would not have had a notochord (though Conclusions
this cannot be ruled out), only that it need not have been The nearly vertical junctions between myomeres in the
the core structure around which the myomeres are orga- putative basal chordate Pikaia gracilens are shown to be
nized. Any number of other axial structures might have indicative of a muscle fiber type more similar to the slow
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fibers of modern chordates than fast fibers. It is not 17. Lacalli TC, Kelly SJ: Ventral neurons in the anterior nerve cord of
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