Nicholas Holland, University of California at San Diego
17 October 2013
The analysis of somite shape in Pikaia by Lacalli raises some interesting points. One that is not directly addressed, however, and where there may be more to say, is whether the authors of the original study, Caron and Conway Morris (CMC), have correctly identified the notochord [see ref. 1 for a detailed history of this unresolved controversy]. The trace interpreted by CMC as notochord lies deep within the body (option 1, the deep notochord hypothesis), about where such a structure would be expected based on its location and function in modern chordates: running roughly at the level of the dorsoventral midpoint of the somite. The functional advantage of this arrangement is presumably to enable the stiffening effect of the notochord to be conveyed more evenly to all parts of the myomere.
The second option, which is historically the first in the Pikaia literature, is to consider the dorsal organ the more likely notochord homolog. Its location, close to the dorsal surface and far from the center of the body, looks awkward to modern eyes, however, and begs the question of where the nerve cord would be located. If the latter is yet more dorsal, it would be both close to the surface of the body (perhaps even intra-epidermal) and distant from the muscles it innervates. In amphioxus, the myomere is innervated by processes extending from the muscles to the surface of the nerve cord rather than by peripheral nerves. If Pikaia were similarly organized, such processes would necessarily have been exceptionally long, which seems an awkward solution. Further, could a notochord in so extreme a dorsal position provide sufficient resistance to muscle contraction across the whole height of the myomere? Lacalli makes the argument that slow swimming, which generates less force than fast swimming, would not require the optimal functioning of the body's support system. A notochord positioned in a fashion that would not work for vertebrates might thus be satisfactory for Pikaia. Interestingly, the prominence of Pikaia myosepta which, from their preservation, must be fairly robust, suggests an alternative: that Pikaia may have relied more on a hydrostatic support system consisting of coelomic chambers with sturdy walls, located close to a surface layer of tissue that is itself comparatively stiff. The latter could be achieved, for example, by having a surface cuticle or epidermal cells strengthened with tonofilaments. The analysis by Lacalli, in my view, suggests more needs to be done to explore alternative explanations of this type. In sum, it might be premature to discard the historically earlier view that the dorsal organ was notochord.
One final comment is prompted by a recent paper [ref. 2] about an acorn worm (Hemichordata, Enteropneusta) that can swim by undulating its trunk, even though that body region has neither a notochord, nor a spacious coelom acting as a hydrostatic skeleton, nor a tough epidermis, cuticle, or exoskeleton that might antagonize contractions of the longitudinal musculature. Perhaps the antagonism to longitudinal contraction is supplied by some sort of coordinated action by circular trunk muscles. In any case, our understanding of the biomechanics of undulatory swimming could well still be somewhat incomplete. From what is known, effective compression struts for opposing longitudinal muscle contraction during undulation can be of several sorts (that might operate in combinations within a given animal). With a better understanding of this subject, one might someday construct evolutionary scenarios without invoking notochord homologs deep in the deuterostome tree.
References
1. Mallatt J, Holland ND: Pikaia gracilens Walcott: Stem chordate, or already specialized in the Cambrian? J Exp Zool B: Mol Dev Evol 2013, 320:247-271.
2. Urata M, Iwasaki S, Ohtsuka S. Biology of the swimming acorn worm Glandiceps hacksi from the Seto Inland Sea of Japan. Zool Sci 2012, 29:305-310.
Competing interests
None declared
More thoughts on notochords
Thurston Lacalli, University of Victoria
17 October 2013
Nick Holland's Comment has prompted me to reflect further on which of the two structures, the putative deep notochord of the original authors (CMC), or the dorsal organ, is the more likely notochord homolog in Pikaia. For my initial analysis of somite shape, I saw no particular reason not to accept the CMC interpretation, but there are caveats that need to be considered.
First, it is important to understand that the chevron shape of chordate myomeres has a developmental origin: somites initially form alongside the notochord, and it's from the latter that inductive signals for muscle formation originate. The myomere then expands dorsally and ventrally by addition of new fibers to its top and bottom margins, but there is a progressive offset, with each new fiber shifted slightly caudal to the previous one. The inflection point in any chevron is therefore aligned with the notochord and marks its location. If any of the comparatively gentle inflections in Pikaia myomeres represent the beginnings of true chevrons, the point where the bend is most pronounced should coincide with the location of the notochord. Though not all the CMC figures are easy to interpret, there appear to be two inflections: a forward one at or just above the level of the deep notochord, and a backward one below the level inferred (though not directly observed) as the location of the alimentary canal. In the former case, the putative deep notochord and the inflection are close enough that they could conceivably coincide. There is, however, no indication of any inflection in somite boundaries as they pass over the dorsal organ. This provides some evidence, though weak, for the CMC interpretation, so long as Pikaia has begun to evolve towards having myomeres that are chevron-shaped. It is weak because the degree of bending is so limited that it could instead reflect processes unrelated to the initial somite/notochord relationship, e.g. later phases of differential growth in surrounding tissues. Conclusion: the issue is unresolved, with no positive evidence from inflection points for the dorsal organ as notochord option.
A second argument against the dorsal organ as notochord is that the nerve cord would then be very dorsal and distant from the muscles it must innervate. The apparent appeal of this view comes from what, I would argue, is a vertebrate bias of seeing the nerve cord as more of an internal structure than it is in basal chordates. Relative to the dorsal fin of adult amphioxus, the nerve cord is displaced somewhat from the dorsal surface. In embryos and larvae, however, the nerve cord is very close to the surface, separated from it only by an axial file of roof plate cells and a thin epithelium. Furthermore, as Ruppert points out [ref 1, pp. 465-469], nerves both entering and leaving the nerve cord are unlike those in vertebrates in being essentially intraepithelial in nature. Ruppert is referring here to the observation that where nerves pass through mesodermal tissues, they appear to do so in a cellular sheath of epithelial origin rather than by penetrating the basal lamina. A thorough survey of the amphioxus nervous system has not been undertaken to determine whether breaches of the latter ever occur, but the amphioxus nerves whose development has been examined do appear to become internalized only secondarily, by enclosure, rather than by growing through mesodermal tissues directly. This is clearly the case for the dorsal nerves: these enter the nerve cord by passing between somites in the adult, but the pathway is pioneered during development by intraepithelial nerves that enter the cord above the level of the somites, and are then enclosed only as the latter grow up around them. Nor do locomotory motor nerves penetrate the basal lamina: their axons remain within the nerve cord, and descend along the basal surface of the neuroepithelium, where they form synapses across the lamina in transit.
In consequence, if you were to reverse the process of neurulation by everting the rather shallow neural tube, and setting aside the secondary enclosures, the amphioxus nervous system would be much closer to an epithelial plexus than a centralized system, little different in essentials from the nervous system of, say, an enteropneust hemichordate. If this is the basal condition rather than something specific to amphioxus, then there is the possibility that ancestral chordates, though they may have had a neural tube, otherwise relied on a superficial plexus of intraepithelial nerves to innervate major end organs. If this were the case with Pikaia, little if any indication of the nervous tissue would be evident in the fossils, and certainly no nerve cord would be expected deep within the body. Conclusion: the amphioxus condition provides some support for the dorsal organ as notochord option in so far as it reduces the need to discover an internal nerve cord and a companion notochord ventral to it.
As a final point, I think it very interesting to entertain the idea of a key role for a hydrostatic support system in Pikaia, via coelomic compartments firmly attached to the integument, given the clear preservation of septa in this fossil. This option further lessens the structural and positional constraints imposed on a notochord if the latter is not required to be the sole means of body support during swimming.
Reference
Ruppert EE: Cephalochordata (Acrania). In Microscopic Anatomy of Invertebrates vol. 15. Edited by Harrison RW, Ruppert EE. Wiley-Liss Inc, New York; 1997:349-504.
Competing interests
No competing interests
Ancient compression struts
Nicholas Holland, University of California at San Diego
12 January 2015
Holland, N. D.
Scripps Institute of Oceanography (UCSD)
The analysis of somite shape in Pikaia by Lacalli raises some interesting points. One that is not directly addressed, however, and where there may be more to say, is whether the authors of the original study, Caron and Conway Morris (CMC), have correctly identified the notochord [ref. 1 includes a history of this unresolved controversy]. The trace interpreted by CMC as notochord lies deep within the body (option 1, the deep notochord hypothesis), about where such a structure would be expected based on its location and function in modern chordates: running roughly at the level of the dorsoventral midpoint of the somit. The functional advantage of this arrangement is presumably to enable the stiffening effect of the notochord to be conveyed more evenly to all parts of the myomere.
The second option, which is historically the first in the Pikaia literature, is to consider the dorsal organ the more likely notochord homolog. Its location, close to the dorsal surface and far from the center of the body, looks awkward to modern eyes, however, and begs the question of where the nerve cord would be located. If the latter is yet more dorsal, it would be both close to the surface of the body (perhaps even intra-epidermal) and distant from the muscles it innervates. In amphioxus, the myomere is innervated by via processes extending from the muscles to the surface of the nerve cord rather than by peripheral nerves. If Pikaia were similarly organized, such processes would necessarily have been exceptionally long, which seems an awkward solution. Further, could a notochord in so extreme a dorsal position provide sufficient resistance to muscle contraction across the whole height of the myomere? Lacalli makes the argument that slow swimming, which generates less force than fast swimming, would not require the optimal functioning of the body¿s support system. A notochord positioned in a fashion that would not work for vertebrates might thus be satisfactory for Pikaia. Interestingly, the prominence of Pikaia myosepta which, from their preservation, must be fairly robust, suggests an alternative: that Pikaia may have relied more on a hydrostatic support system consisting of coelomic chambers with sturdy walls, located close to a surface layer of tissue that is itself comparatively stiff. The latter could be achieved, for example, by having a surface cuticle or epidermal cells strengthened with tonofilaments. The analysis by Lacalli, in my view, suggests more needs to be done to explore alternative explanations of this type. In sum, it might be premature to discard the historically earlier view that the dorsal organ was notochord.
One final comment is prompted by a recent paper [ref. 2] about an acorn worm (Hemichordata, Enteropneusta) that can swim by undulating its trunk, even though that body region has neither a notochord, nor a spacious coelom acting as a hydrostatic skeleton, nor a tough epidermis, cuticle, or exoskeleton that might antagonize contractions of the longitudinal musculature. Perhaps the antagonism to longitudinal contraction is supplied by some sort of coordinated action by circular trunk muscles. In any case, our understanding of the biomechanics of undulatory swimming could well still be somewhat incomplete. From what is known, effective compression struts for opposing longitudinal muscle contraction during undulation can be of several sorts (that might operate in combinations within a given animal). A better understanding of this subject would be helpful for functional interpretations of fossils deep in the deuterostome tree.
References
1. Mallatt J, Holland ND: Pikaia gracilens Walcott: Stem chordate, or already specialized in the Cambrian? J Exp Zool B: Mol Dev Evol 2013, 320:247-271.
2. Urata M, Iwasaki S, Ohtsuka S. Biology of the swimming acorn worm Glandiceps hacksi from the Seto Inland Sea of Japan. Zool Sci 2012, 29:305-310.
EvoDevo
Ancient compression struts
17 October 2013
The analysis of somite shape in Pikaia by Lacalli raises some interesting points. One that is not directly addressed, however, and where there may be more to say, is whether the authors of the original study, Caron and Conway Morris (CMC), have correctly identified the notochord [see ref. 1 for a detailed history of this unresolved controversy]. The trace interpreted by CMC as notochord lies deep within the body (option 1, the deep notochord hypothesis), about where such a structure would be expected based on its location and function in modern chordates: running roughly at the level of the dorsoventral midpoint of the somite. The functional advantage of this arrangement is presumably to enable the stiffening effect of the notochord to be conveyed more evenly to all parts of the myomere.
The second option, which is historically the first in the Pikaia literature, is to consider the dorsal organ the more likely notochord homolog. Its location, close to the dorsal surface and far from the center of the body, looks awkward to modern eyes, however, and begs the question of where the nerve cord would be located. If the latter is yet more dorsal, it would be both close to the surface of the body (perhaps even intra-epidermal) and distant from the muscles it innervates. In amphioxus, the myomere is innervated by processes extending from the muscles to the surface of the nerve cord rather than by peripheral nerves. If Pikaia were similarly organized, such processes would necessarily have been exceptionally long, which seems an awkward solution. Further, could a notochord in so extreme a dorsal position provide sufficient resistance to muscle contraction across the whole height of the myomere? Lacalli makes the argument that slow swimming, which generates less force than fast swimming, would not require the optimal functioning of the body's support system. A notochord positioned in a fashion that would not work for vertebrates might thus be satisfactory for Pikaia. Interestingly, the prominence of Pikaia myosepta which, from their preservation, must be fairly robust, suggests an alternative: that Pikaia may have relied more on a hydrostatic support system consisting of coelomic chambers with sturdy walls, located close to a surface layer of tissue that is itself comparatively stiff. The latter could be achieved, for example, by having a surface cuticle or epidermal cells strengthened with tonofilaments. The analysis by Lacalli, in my view, suggests more needs to be done to explore alternative explanations of this type. In sum, it might be premature to discard the historically earlier view that the dorsal organ was notochord.
One final comment is prompted by a recent paper [ref. 2] about an acorn worm (Hemichordata, Enteropneusta) that can swim by undulating its trunk, even though that body region has neither a notochord, nor a spacious coelom acting as a hydrostatic skeleton, nor a tough epidermis, cuticle, or exoskeleton that might antagonize contractions of the longitudinal musculature. Perhaps the antagonism to longitudinal contraction is supplied by some sort of coordinated action by circular trunk muscles. In any case, our understanding of the biomechanics of undulatory swimming could well still be somewhat incomplete. From what is known, effective compression struts for opposing longitudinal muscle contraction during undulation can be of several sorts (that might operate in combinations within a given animal). With a better understanding of this subject, one might someday construct evolutionary scenarios without invoking notochord homologs deep in the deuterostome tree.
References
1. Mallatt J, Holland ND: Pikaia gracilens Walcott: Stem chordate, or already specialized in the Cambrian? J Exp Zool B: Mol Dev Evol 2013, 320:247-271.
2. Urata M, Iwasaki S, Ohtsuka S. Biology of the swimming acorn worm Glandiceps hacksi from the Seto Inland Sea of Japan. Zool Sci 2012, 29:305-310.
Competing interests
None declared
More thoughts on notochords
17 October 2013
Nick Holland's Comment has prompted me to reflect further on which of the two structures, the putative deep notochord of the original authors (CMC), or the dorsal organ, is the more likely notochord homolog in Pikaia. For my initial analysis of somite shape, I saw no particular reason not to accept the CMC interpretation, but there are caveats that need to be considered.
First, it is important to understand that the chevron shape of chordate myomeres has a developmental origin: somites initially form alongside the notochord, and it's from the latter that inductive signals for muscle formation originate. The myomere then expands dorsally and ventrally by addition of new fibers to its top and bottom margins, but there is a progressive offset, with each new fiber shifted slightly caudal to the previous one. The inflection point in any chevron is therefore aligned with the notochord and marks its location. If any of the comparatively gentle inflections in Pikaia myomeres represent the beginnings of true chevrons, the point where the bend is most pronounced should coincide with the location of the notochord. Though not all the CMC figures are easy to interpret, there appear to be two inflections: a forward one at or just above the level of the deep notochord, and a backward one below the level inferred (though not directly observed) as the location of the alimentary canal. In the former case, the putative deep notochord and the inflection are close enough that they could conceivably coincide. There is, however, no indication of any inflection in somite boundaries as they pass over the dorsal organ. This provides some evidence, though weak, for the CMC interpretation, so long as Pikaia has begun to evolve towards having myomeres that are chevron-shaped. It is weak because the degree of bending is so limited that it could instead reflect processes unrelated to the initial somite/notochord relationship, e.g. later phases of differential growth in surrounding tissues. Conclusion: the issue is unresolved, with no positive evidence from inflection points for the dorsal organ as notochord option.
A second argument against the dorsal organ as notochord is that the nerve cord would then be very dorsal and distant from the muscles it must innervate. The apparent appeal of this view comes from what, I would argue, is a vertebrate bias of seeing the nerve cord as more of an internal structure than it is in basal chordates. Relative to the dorsal fin of adult amphioxus, the nerve cord is displaced somewhat from the dorsal surface. In embryos and larvae, however, the nerve cord is very close to the surface, separated from it only by an axial file of roof plate cells and a thin epithelium. Furthermore, as Ruppert points out [ref 1, pp. 465-469], nerves both entering and leaving the nerve cord are unlike those in vertebrates in being essentially intraepithelial in nature. Ruppert is referring here to the observation that where nerves pass through mesodermal tissues, they appear to do so in a cellular sheath of epithelial origin rather than by penetrating the basal lamina. A thorough survey of the amphioxus nervous system has not been undertaken to determine whether breaches of the latter ever occur, but the amphioxus nerves whose development has been examined do appear to become internalized only secondarily, by enclosure, rather than by growing through mesodermal tissues directly. This is clearly the case for the dorsal nerves: these enter the nerve cord by passing between somites in the adult, but the pathway is pioneered during development by intraepithelial nerves that enter the cord above the level of the somites, and are then enclosed only as the latter grow up around them. Nor do locomotory motor nerves penetrate the basal lamina: their axons remain within the nerve cord, and descend along the basal surface of the neuroepithelium, where they form synapses across the lamina in transit.
In consequence, if you were to reverse the process of neurulation by everting the rather shallow neural tube, and setting aside the secondary enclosures, the amphioxus nervous system would be much closer to an epithelial plexus than a centralized system, little different in essentials from the nervous system of, say, an enteropneust hemichordate. If this is the basal condition rather than something specific to amphioxus, then there is the possibility that ancestral chordates, though they may have had a neural tube, otherwise relied on a superficial plexus of intraepithelial nerves to innervate major end organs. If this were the case with Pikaia, little if any indication of the nervous tissue would be evident in the fossils, and certainly no nerve cord would be expected deep within the body. Conclusion: the amphioxus condition provides some support for the dorsal organ as notochord option in so far as it reduces the need to discover an internal nerve cord and a companion notochord ventral to it.
As a final point, I think it very interesting to entertain the idea of a key role for a hydrostatic support system in Pikaia, via coelomic compartments firmly attached to the integument, given the clear preservation of septa in this fossil. This option further lessens the structural and positional constraints imposed on a notochord if the latter is not required to be the sole means of body support during swimming.
Reference
Ruppert EE: Cephalochordata (Acrania). In Microscopic Anatomy of Invertebrates vol. 15. Edited by Harrison RW, Ruppert EE. Wiley-Liss Inc, New York; 1997:349-504.
Competing interests
No competing interests
Ancient compression struts
12 January 2015
Holland, N. D.
Scripps Institute of Oceanography (UCSD)
The analysis of somite shape in Pikaia by Lacalli raises some interesting points. One that is not directly addressed, however, and where there may be more to say, is whether the authors of the original study, Caron and Conway Morris (CMC), have correctly identified the notochord [ref. 1 includes a history of this unresolved controversy]. The trace interpreted by CMC as notochord lies deep within the body (option 1, the deep notochord hypothesis), about where such a structure would be expected based on its location and function in modern chordates: running roughly at the level of the dorsoventral midpoint of the somit. The functional advantage of this arrangement is presumably to enable the stiffening effect of the notochord to be conveyed more evenly to all parts of the myomere.
The second option, which is historically the first in the Pikaia literature, is to consider the dorsal organ the more likely notochord homolog. Its location, close to the dorsal surface and far from the center of the body, looks awkward to modern eyes, however, and begs the question of where the nerve cord would be located. If the latter is yet more dorsal, it would be both close to the surface of the body (perhaps even intra-epidermal) and distant from the muscles it innervates. In amphioxus, the myomere is innervated by via processes extending from the muscles to the surface of the nerve cord rather than by peripheral nerves. If Pikaia were similarly organized, such processes would necessarily have been exceptionally long, which seems an awkward solution. Further, could a notochord in so extreme a dorsal position provide sufficient resistance to muscle contraction across the whole height of the myomere? Lacalli makes the argument that slow swimming, which generates less force than fast swimming, would not require the optimal functioning of the body¿s support system. A notochord positioned in a fashion that would not work for vertebrates might thus be satisfactory for Pikaia. Interestingly, the prominence of Pikaia myosepta which, from their preservation, must be fairly robust, suggests an alternative: that Pikaia may have relied more on a hydrostatic support system consisting of coelomic chambers with sturdy walls, located close to a surface layer of tissue that is itself comparatively stiff. The latter could be achieved, for example, by having a surface cuticle or epidermal cells strengthened with tonofilaments. The analysis by Lacalli, in my view, suggests more needs to be done to explore alternative explanations of this type. In sum, it might be premature to discard the historically earlier view that the dorsal organ was notochord.
One final comment is prompted by a recent paper [ref. 2] about an acorn worm (Hemichordata, Enteropneusta) that can swim by undulating its trunk, even though that body region has neither a notochord, nor a spacious coelom acting as a hydrostatic skeleton, nor a tough epidermis, cuticle, or exoskeleton that might antagonize contractions of the longitudinal musculature. Perhaps the antagonism to longitudinal contraction is supplied by some sort of coordinated action by circular trunk muscles. In any case, our understanding of the biomechanics of undulatory swimming could well still be somewhat incomplete. From what is known, effective compression struts for opposing longitudinal muscle contraction during undulation can be of several sorts (that might operate in combinations within a given animal). A better understanding of this subject would be helpful for functional interpretations of fossils deep in the deuterostome tree.
References
1. Mallatt J, Holland ND: Pikaia gracilens Walcott: Stem chordate, or already specialized in the Cambrian? J Exp Zool B: Mol Dev Evol 2013, 320:247-271.
2. Urata M, Iwasaki S, Ohtsuka S. Biology of the swimming acorn worm Glandiceps hacksi from the Seto Inland Sea of Japan. Zool Sci 2012, 29:305-310.
Competing interests
no competing interests