Approach #5. Examining the morphology of existing organisms
This approach is limited by the fact that animals that evolve while remaining within a particular ecological niche replace their ancestrial types, so that the ancestrial types are not represented in the present-day fauna.
What are intermediate organisms, from the standpoint of actin-myosin based locomotion?
Dictyostelium . The pseudoplasmodium moves by the cooperative action of many amoebae, at speeds up to 1 mm/hr. There is no evidence for waves of contraction. Locomotion simply seems to be the result of the aggregate amoeboid locomotion of the individual cells. Individual amoebae can move at 4-5 mm/day. (Bonner et al., Mycologia 45: 235)
Porifera. Some sponges can glide slowly (4 mm/day) over a substrate. This appears to be no more advanced than Dictyostelium , just caused by the amoeboid locomotion of cells at the base of the sponge, without any contractile waves. (Bond & Harris, J exp Zool 246:271-284 (1988)) Contractile cells containing lots of parallel microtubules and microfilaments occur in sponges to close the osculum, but they are not involved in locomotion. There are many other features of sponges that are at a simpler level than other multicellular animals. The similarity between the choanocytes of sponges and the free-living choanoflagellates has been considered to be stronger than any similarities of sponges to other Metazoa. For these reasons, sponges have traditionaly been considered to be the result of an independent line of evolution, without much relationship to other Metazoa. More recent molecular evolution studies, however, are supporting a closer relationship between Porifera and other Metazoa, and suggest that the choanoflagellates may be the closest living unicellular ancestor of the Metazoa.
What these examples tell us is that multicellular organization, and very slow locomotion, can evolve before the differentiation of contractile cells that are used for locomotion . Once this stage is reached, it is easy to imagine that natural selection could lead to improved locomotion involving waves of cell contraction rather than amoeboid locomotion. (Note that flatworms and other small multicellular animals using cilia can achieve speeds of 1-2 mm/sec that are comparable to speeds of small animals using waves of muscle contraction.)
Cnidarians. These have contractile cells, and some anatomically defined muscles,
nerves, and skeletal elements. Contraction appears to involve the same mechanisms
found in muscles of other animals, but, as already mentioned, acetylcholine is not
used as a neurotransmitter. They are not "worms", because they do not have the cephalization
and bilateral symmetry that is associated with crawling over a surface and looking
for food. The unanswered questions: Did they have worm-like ancestors, and lose
their worm-like features when they evolved in the direction made possible by nematocysts?
Or have nematocysts allowed them to survive, while maintaining primitive features
of animals before the "worm" stage?
Acoela. Proponents of cellularization theories have often emphasized the existence
of a group of small, free-living, Turbellarian flatworms, known as the Acoela.
They live in marine sediments and are typically:
Small: 1-2 mm long; often have syncytial (multinucleate) tissues;
Move only by cilia
Little or no parenchynma between epidermis and an interior mass of endodermal cells.
Mouth on ventral surface, but no real gut cavity (hence name of group). Endodermal cells feed individually by phagocytosis.
Very little cephalization
The proponents of cellularization theories have emphasized the similarity between Acoela and protozoa such as Paramecium or Opalina .
But: the Acoela have some features that are nearly as complicated as in other flatworms, especially the reproductive organs, and also some features of the nervous system and the presence of simple eyes. These are part of the reason for classifying them with other flatworms. They have some small muscle cells, of unknown function. They may have evolved from more complicated flatworms by loss of features. At best, they should just be thought of as a model that provides evidence that simple animals with these features are possible, and can survive as free-living organisms.
Cellularization theories suggest that evolution proceeded from a large, multinucleate, ciliated or flagellated cell, by cellularization to a rather similar multicellular animal that also relied on cilia for locomotion. As long as they remained that small, locomotion by cilia was probably more effective than locomotion by contractile waves. However, to become large and fully exploit the advantages of multicellularity, locomotion by contractile cells had to evolve. This scheme suggests that the gradual evolution of multicellular organisms did not involve a gradual transition from amoeboid locomotion to muscular locomotion.
A closer examination of how worms move helps us understand how muscular locomotion may have evolved.
Muscle antagonism can be achieved without the use of rigid,jointed skeletons
Hydrostatic skeletons. An excellent example is provided by Urechis :
A good example of a simple, but not primitive, burrowing worm is Urechis caupo , a member of the Phylum Echiuroidea. Urechis lives in U-shaped burrows in sandy or muddy substrata, pumping water in one end of the U-shaped tube and out the other end, and using a mucous net to filter suspended food particles out of the water current. It uses peristaltic contractions to pump water through the tube. It uses retrograde contractile waves to move around in its tube, and to enlarge its tube by burrowing through the substratum. These movements are generated by two sets of muscles in the body wall:
Circular muscles, running around the circumference of the animal, outside of the longitudinal muscles.
This muscular body wall surrounds a fluid filled cavity, making up most of the volume of the animal. This fluid filled cavity acts as a hydrostatic skeleton . All of the muscles of the body wall will tend to increase the pressure in the body cavity when they contract, so they are all antagonistic to each other. Normally, when the animal is active, they are all in a state of contraction that maintains a pressure in the body cavity. Localized relaxation is used to allow elongation of specific groups of muscles:
Peristaltic contractions are produced by waves of relaxation involving only the circular muscles. The result is that bulges move along the body, without any locomotion.
Retrograde waves are produced by a combination of relaxation of circular muscles, producing bulges, and relaxation of longitudinal muscles at the anterior side of a backward propagating bulge. This causes the regions between the bulges to move forward relative to the substratum. Traction is maintained by pressure of the bulges against the walls of the tube.
Measurements on burrowing animals have shown that this mechanism can generate significant forces at the anterior end, allowing the animal to push through the substratum.
Urechis is an example of a highly evolved animal specialized for burrowing, with a well-developed hydrostatic skeleton and a nervous system for muscular control. How did this arrangement evolve?
Many animals crawl by means of muscular waves called pedal locomotory waves . This form of locomotion is found in larger flatworms, in sea anemones, and in many molluscs (chitons and gastropods).
--Retrograde waves of contraction of longitudinally oriented muscles pass backwards along the ventral surface.
--contracted regions adhere to the substratum.
--relaxed regions are pulled forward over the surface and elongate, at the anterior end of a bulge, as the wave passes. As a result, the animal moves forward relative to the bulges that contact the substratum.
As described in the McNeill Alexander text, the peculiar properties of mucous are important in facilitating the locomotion of present-day animals by pedal locomotory waves. The mucous allows the body surface to slide easily over the substratum in high stress regions, where the force of muscle contraction is applied to a small surface area. We can speculate that this mechanism was used in the early evolution of this form of locomotion, but this will be difficult to prove. Simple bulging out of the contracted muscle cells, because they individually maintain a constant volume, might have been an easier, but less efficient, starting point.
Some existing animals use another solution to this problem, that might have been useful for very primitive animals. They make use of the fact that the spaces between the bottom of the foot and the substratum can be enclosed at the edges of the foot to contain a fluid-filled cavity of constant volume. Consequently, any muscular contraction that attempts to compress the volume of this cavity can cause antagonistic elongation of relaxed muscles surrounding the cavity. It is an extracorporeal form of a hydrostatic skeleton.
What causes the propagated contractile wave?
In existing animals, even in these simple movements, the muscular contractions are controlled by the nervous system. However, we have evidence for simpler possibilities:
--muscle cells can propagate electrical signals, as in vertebrate heart muscle.
--epithelial cells can propagate electrical signals. This has been found in Cnidaria.
--muscle contraction can be stimulated by stretch induced by the contraction of adjacent cells. This stretch sensitivity is a major feature of some muscles, and is especially important in some insect flight muscles. Stretch-induced contraction is important in peristaltic movement of vertebrate intestines, although in this case there are nerve cells involved, not just the muscle cells.
Although we don't know of an existing case where just these more primitive capabilities are used to control locomotory waves, it is plausible to hypothesize that they were used by primitive multicellular animals before the evolution of nervous systems. We can conclude that pedal locomotory waves could have easily evolved using only longitudinal contractile elements, to enable larger, bottom-crawling animals to move more effectively than would be possible by ciliary or amoeboid locomotion.
As the mechanisms for pedal locomotory waves were improved by further evolution, one of the improvements may have been the development of contraction capability perpendicular to the longitudinal muscles. This might assist the regions where longitudinal muscles are relaxing to raise away from the substrate, and assist the elongation of these muscles at the same time. This would easily lead to two sets of muscles, one of which which would operate out of phase with the other set as the wave propagates. This would probably require the development of a 2nd conduction system, which might have been easier if the longitudinal and circular muscle cells were in clearly separate sheets, allowing conduction by muscle cells before a nervous system appeared.
[The existence of these two orthogonal muscle sets allows a different kind of pedal locomotory wave. The retrograde waves already discussed propagate backwards, while the animal moves forward. Some snails use direct waves, which move forward on the foot. In these waves, both muscle sets contract at the same time, lifting the longitudinally contracted regions away from the substratum. As the wave passes forwards, longitudinal contraction at the posterior edges of the bulged regions in contact with the substratum pulls the raised regions forwards -- so the animal moves forwards. Actually, in snails, the two muscle sets are not longitudinal and vertical, but are inclined \ / .]
The evolution of these two orthogonal muscle sets, in order to facilitate locomotion by pedal locomotory waves, can be viewed as a preadaptation for the use of these orthogonal muscle sets for a new function -- burrowing in the substratum.
The development of distinct circular and longitudinal muscles, and a body cavity allowing these muscles to be antagonistic via a hydrostatic skeleton, led to the evolution of burrowing animals able to exploit niches within the substratum.
The ability to burrow in this manner opens up a new range of ecological niches into which some evolutionary lines can move, to escape competition with animals living on the surface. Burrowing animals can use the substratum for protection, as in the case of Urechis , or they can use it as a source of food, as an earthworm does. This capability is utilized by members of several invertebrate phyla:
Cnidarians (in the class Anthozoa) burrowing sea anemones.
Echinoderms (in the class Holothuroidea) "sea cucumbers"
Annelids, Sipunculoidea, Priapuloidea, etc.
The same principle is used by non-burrowing animals:
The stalk of most polyps; Siphons of bivalves; gut peristalsis
The use of circular and longitudinal muscles and a hydrostatic skeleton by these animals is one very important example of how soft-bodied animals have solved the problems of using muscles efficiently, without the benefits of the rigid, jointed, skeletons seen in arthropods and vertebrates.
Some diversions: Other uses of hydrostatic skeletons:
For swimming :
The most primitive swimming movements are probably seen in the undulatory waves that flatworms use for swimming. The additional problem here is the conversion of muscular contraction into bending of the body. The solution requires some compression-resistant skeletal elements, so that the body doesn't just shorten when muscles on one side of the body contract. In flatworms, this compression resistance is a rather unspecialized property of the part of the worm that is not contracting, resulting from the maintenance of constant cell volumes.
Nematodes swim by undulations of the body in the dorsal-ventral plane. These worms have longitudinal muscles just underneath the body surface. There are no circular muscles, but there is a fibrous cuticle that resists radial expansion. Since radial expansion is prevented, the body cannot shorten and maintain a constant volume, so the fibrous cuticle provides prevents shortening of the animal when the longitudinal muscles contract. In other words, the fibrous cuticle provides compression resistance. If longitudinal muscles on one side of the body contract, the body must bend. The whole interior of the animal, inside the fibrous cuticle, acts as a hydrostatic skeleton.
Primitive chordates contain an axial skeletal element called the notochord . This is equivalent in its properties to a fluid-filled rod with a fibrous sheath, although it is really made up of a mass of cells surrounded by a fibrous sheath. It provides compression resistance in the same manner as the nematode cuticle and hydroskeleton, but here the muscles are on the outside of the sheath, rather than inside. Also, in this case there are side-to-side undulations for swimming.
Nemertean worms, and some others, have a proboscis that can be rapidly extended to capture food. Typically, there is a fluid-filled proboscis cavity, in which the proboscis is stored in an inside-out configuration. When muscles around the proboscis cavity contract, the increased pressure causes the proboscis to evert. These muscles are typically antagonized by a proboscis retractor muscle running from the back of the cavity through to the tip of the proboscis.
Most groups of Echinoderms have tube feet . These are used for locomotion, attachment, and food capture. The tubular podium extends through openings in the skeleton. Its wall contains circumferential fibrous elements that prevent an increase in radius, and longitudinal muscles that can cause contraction or bending of the tube foot. These muscles are antagonized by muscles surrounding the ampula, inside the skeleton; when they contract, fluid is pushed into the podium, so that the podium extends.
Antagonism by elastic structures:
Cnidarian medusae typically have muscles in the oral surface of the disc and around the edge of the disc. Their contraction causes the animal to move in the aboral direction, by pushing water back. They are antagonized not by another set of muscles, but by the general elasticity of the mesoglea. In Polyorchis , there is also a clear set of radial elastic fibers between the outer, aboral surface and the inner, oral surface lining the subumbrellar cavity, which antagonizes the contraction of muscles running circularly around the cavity in the innerwall.
Another excellent example is the hinge ligament of bivalve molluscs, a compression pad that causes the shell to open when the closer muscles relax. Some clams even use this opening and closing action for swimming. The hinge ligament contains a high concentration of fibers of an elastic protein called abducin . Other elastic proteins are resilin , in insects, and elastin , in vertebrates. Elastic proteins generally contain large numbers of alanines and glycines. Abducin and resilin appear to be examples of rubber-like elasticity, resulting from the tendency of the polypeptide chains to adopt "random coil" configurations and resist extension. Elastin appears to have a more complicated "coiled-coil" configuration.
A general problem of soft-bodied animals is the problem of sucking water into the animal -- this is made difficult by the fact that muscles can only contract.
Sea anemones solve this problem by using cilia to pump water into the gastrocoel for expansion, after the animal has been contracted by muscular contraction and expulsion of water through the mouth. Special tracts of cilia, called siphonglyphs , are at either side of the mouth for this purpose.
Several animals use radial muscles to draw water into the body:
radial muscles in the squid mantle; plus radial elastic fibers.
radial muscles in the pharynx of Navanax
radial muscles in the cloaca of Urechis
To return to thinking about phylogeny, I have presented the way in which a fluid-filled internal body cavity (or, in Cnidarians, a gut cavity) can be used as a hydraulic skeleton, to facilitate locomotion and other muscular actions. Fluid-filled internal body cavities can also be used for other functions, especially for :
"Space" for expansion and movement of other organs. For example, the abdominal organs of humans are suspended in an abdominal cavity containing a small amount of "peritoneal fluid".
Storage. For example, the body cavity of Urechis , in addition to functioning as a hydrostatic skeleton, contains many "red blood cells" that use hemoglobin to store oxygen. (Urechis also has a separate circulatory system, with a colorless fluid.) In many annelids, the body cavities of the posterior segments are used to accumulate and store gametes before release.
The characteristics of the primary body cavity are often used to describe particular groups of animals:
Platyhelminthes (flatworms) are called Acoelomate . Their only interior spaces are gut, excretory tubules, reproductive ducts. This condition has traditionally been considered primitive, indicating that Platyhelminthes are the closest living representatives of the earliest bilaterally symmetric Metazoa, and newer molecular evolution studies are supporting this idea.
Nemertea (ribbon worms) have also been described as Acoelomate, because they do not have a "primary body cavity" that serves as a hydrostatic skeleton for locomotion. However, the body contains loose parenchymaceous tissue that en mass can act as a hydroskelton for antagonism between body wall muscles. Most of the burrowing is done with the proboscis, which has a more efficient hydroskeleton. They have a variety of more advanced features such as a circulatory system. Newer molecular evolution studies indicate that they are not closely related to Platyhelminthes, and should be grouped with more advanced, coelomate, Protostomes.
Nematodes are called Pseudocoelomate . Their interior body cavity is simply a space between the ectodermal and endodermal derivatives, that can be be traced through development as a derivative of the blastocoel of the early embryo.
Rotifers, and several other minor phyla, are also categorized as Pseudocoelomate. However, this probably is not a sufficient basis to think that there is any evolutionary relationship between these phyla. The idea that the Pseudocoelomate condition is an evolutionary stage between the Acoelomate condition and the possession of a true coelom is not supported by recent molecular evolution studies.
Annelids and Urechis are good examples of animals that have a body cavity that functions as a hydroskeleton and is considered to be a true coelom . They are therefore called Coelomate or Eucoelomate.
A true coelom is a body cavity formed by mesodermal tissue, which retains an epthelial lining of mesodermal tissue (peritoneum).
Chordates have a body cavity (or cavities) in which the internal organs are suspended, but it does not serve as a hydrostatic skeleton for locomotion, because this function has been provided for by the notochord or the skeleton of cartilage or bone.
It fits the definition of a true coelom.
Echinoderms also have a true coelom that serves for both circulation and hydroskeletal functions.
In Arthropods, the primary body cavity is a haemocoele that serves as part of the circulatory system. It may function as a hydroskeleton in some cases, but the exoskeleton provides most of the skeletal functions needed by Arthropods. There are no cavities fitting the definition of a coelom except for parts of the reproductive systems. However, Arthropods have been traditionally considered to be Coelomate animals, because they were believed to have evolved from ancestrial groups that were closely related to Annelids. This is probably a very weak argument, because it is difficult to exclude the possibility that the coelom of Annelids appeared after the evolutionary divergence of Annelids and Arthropods.
Most molluscs also have a haemocoel as the primary body cavity, serving for circulation and sometimes for hydroskeletal functions. However, they usually also have a coelomic cavity surrounding the heart and sometimes other organs. This is especially well developed in Cephalopods. The true coelom does not function as a hydroskeleton, and there is no evidence that it ever did.
Is the possession of a coelom an important phylogenetic characteristic?
One view is that the coelom is an important evolutionary invention, that appeared only once, or very few times, and therefore links together coelomate phyla. It may have originally evolved to solve the problem of providing for a hydrostatic skeleton in burrowing worms. It turned out to be valuable for other purposes, and therefore it is a characteristic of higher groups, such as the Vertebrates. Proponents of this view would say that the coelomic spaces of Molluscs and Arthropods are the remnants of an ancestrial hydroskeletal coelom. This view suggests that the evolution of an efficient (coelomic) body cavity as a hydrostatic skeleton for burrowing was a preadaptation that made possible the use of coeloms for other functions in the descendents of early burrowing animals.
The opposing view is that the most successful phyla are those that have discovered ways to use mesodermal tissue for a variety of new functions. Coelomic cavities are just one example of what can be done with mesoderm. They are so simple that they could have evolved independently many times, whenever they were needed for a particular function. They are therefore of no use for reconstructing phylogeny.
Did metamerisim first appear in a burrowing coelomate animal in order to increase the efficiency of burrowing?
Segmentation , also known as metamerism , is characteristic of Annelids and Arthropods, and therefore of the vast majority of animal species. We can speculate that it is an important reason for the success of these groups, so it is important to understand it.
One view is that metamerism first appeared in a burrowing animal with a hydroskeleton, in order to increase the efficiency of burrowing.
The argument is that a worm with a single body cavity, like Urechis , can use its circular and longitudinal muscles for pumping and occasional burrowing movements, for example to excavate a semi-permanent tube. In order to burrow continously in search of food, like an earthworm does, it needs a more efficient musculoskeletal arrangement. The partitioning of the body cavity by septa into a longitudinal series of compartments tends to isolate the effects of local contractions and elongations, leading to more efficient burrowing movements. In an earthworm, the septa are not rigid enough to completely isolate each segment from its neighbors, but the cumulative effect over many segments is enough to isolate the activity of different parts of the worm.
The importance of metamerism is believed to be its facilitation of the differentiation of different regions of the body for different functions, as strongly exemplified by the Arthropods. The origin of metamerism as a means for increasing burrowing efficiency can be viewed as a preadaptation that provided a basis for the extensive elaboration of segmentatal differention by Arthropods.
The proponents of this view also argued that the different, and milder, segmentation of the vertebrate body arose independently, but was also initially an adaptation to facilitate undulatory swimming locomotion by establishing easily controlled subgroups of muscles along the body.
The recent discoveries of similar genes and regulatory elements involved in the control of axial organization throughout the Metazoa suggests, instead, that the developmental mechanisms responsible for metamerism may be a very basic part of the development of all Metazoa, which is expressed in different ways and to different degrees in various phyla. This, and other, newer information is challenging the traditional view that Arthropods have inherited their metamerism from their Annelid ancestors.
Protostomes and Deuterostomes are considered to be two major subgroups of coelomate Metazoa, representing two distinct phylogenetic lines.
Annelids, Molluscs, and Arthropods are the three major groups that are traditionally called Protostomes, based on:
Adults with a body organization in which the longitudinal nerve cord is ventral to the gut.
Exoskeletons and chitin.
Very strong similarities in early embryology of marine molluscs and annelids.
In the past, the metamerism of Annelids and Arthropods was considered to be a feature linking them together into this group, but this now appears to be a weak argument.
Echinoderms and Chordates are the two major phyla that are traditionally called Deuterostomes; a minor phylum, the Hemichordata, helps to link these two major phyla together.
Adults have a body organization with a dorsal nerve cord, sometimes formed by ectodermal invagination.
Chitin is rare or absent, and skeletons are typically endoskeletons.
Strong similarities in early embryology of echinoderms and hemichordates, clearly different from annelid and mollusc patterns.
Trying to fit the other, minor Metazoan phyla into this dichotomy has been difficult or impossible. Although their existence weakens the argument that these are two distinct phylogenetic lines, the use of Protostome and Deuterostome as descriptive terms is still very useful and common.
Many of the ideas in this section were derived from the book by R. B. Clark (1964) "Dynamics in Metazoan Evolution", Oxford University Press.