Lecture 6 Sept. 24

1. Lecture 6 Sept. 24 Thomson’s Gazelle Encyclopedia Britannica My cow ramble of last lecture actually means something. Close, careful, thoughtful, observation of behaviour and form is the way to infer function. Naturally selected for running; artificially selected for milk production. Macleans Alert posture of a gazelle signals to conspecifics ‘be ready to run’.

2. Coelom as fluid skeleton: hydrostatic skeleton with antagonistic muscles: stress (force per unit area) translocated by fluid • Observe an annelidan, a segmented worm (Phylum Annelida) and query its morphology. • A tube within a tube, the body wall two layers of muscle with fibres running 90 degrees to each other, chaetae (pointy things indeed) protruding from the wall: can be protracted and retracted; septa bulkheads invested with transverse muscle etc. • Ask questions: why segments?, why a fluid space?, why chaetae, why a kidney pair in each segment? Why muscle on septa?etc.

3. What is a coelom? It is defined as a fluid-filled cavity forming during development within the early differentiated tissue mesoderm. Animals with a coelom (segmented worms) are called coelomate; animals without one (flatworms) are acoelomate. Some animals (nematodes) have a fluid-filled cavity that is not homologous with the coelom: called a pseudocoelom. chaetae Why chaetae? Think about where an earthworm lives. Within soil, burrowing, searching out softer places and crevices, going around roots & rocks. The worm needs to twist and turn and push its body. For push you need purchase. For this it has the chaetae, functioning as hobnails or crampons. For burrowing you need a cylindrical body – no corners.

4. Gaining ground occurs all along the body, at each constriction (yellows) ahead of the anchored (greens). Peristalsis is a term applied to guts as well as worm body walls: a dilation followed by a constriction: peristalsis in the worm’s gut pushes boluses of food (being digested) along the tubular tract.

5. Kier on annelid locomotion, p1250. Why segments, why septa? • Circular vs longitudinal muscles, peristalsis (waves) – features of a number of ‘worm-like’ (vermiform) animals: includes holothurian echinoderms (sea cucumbers). • “In annelids such as the earthworm, the coelom is divided into segments by muscular septa, which prevent movement of the hydrostatic fluid from one segment to the other during normal locomotion…subdivision of the coelom allows individual segments to operate independently, thereby facilitating localized action…” • “Septa are likely crucial in allowing large lateral forces to be exerted during burrowing” • ‘Kier’s Law’ “at a given [coelomic fluid] pressure [internally expressed stress] the stresses in the circumferential direction are twice those in the longitudinal direction.” Yet the volume devoted to circular muscle is not greater: “…the area of the longitudinal muscles is …greater [than that of the circular]. Because there is relatively more longitudinal muscle “the resulting pressures produced by the longitudinal muscles may be as much as 5 to 20 times greater than those produced by the circular muscles.”

6. “at a given pressure, the stresses in the circumferential direction {hoop stress of McCurley} are twice those in the longitudinal direction.” “...the volume of the longitudinal muscles is greater [than the circular]” “...the resulting pressure produced by the longitudinal muscles may be as much as 5-20 times greater than those produced by the circular muscles” This is adaptive in obtaining purchase, i.e., less force is needed to contract circulars and reach a part of the body forward or backward.

7. “The septa are thought to allow the pressure to be different in one …compartment… compared with another (without septa [imagine it as isn’t] an increase in pressure would be transmitted along the entire length of the body); thus the high pressure of a localized maximal contraction of the longitudinal muscle (perhaps required to enlarge the burrow*) will not be transmitted down the length of the worm and overwhelm the circular muscle in another part of the body” (Kier p.1251) • *or better just to get the purchase for normal movement through soil • We then come to Nematode worms: • “…example of the importance of connective tissues [inextensible collagen fibres are major components of connective tissue] for the hydrostatic skeleton • Nematodes possess robust longitudinal muscle bundles, but they lack the circular muscle fibres that typically serve as antagonists in other hydrostatic animal skeletons. How then, can the longitudinal musculature be antagonized?” – especially by a fibre, collagen, that is inextensible.

8. “…if all the matter in the universe except the nematodes were swept away, our world would still be dimly recognizable, and if, as disembodied spirits, we could then investigate it, we should find its mountains, hills, vales, rivers, lakes and oceans represented by a film of nematodes. The location of towns would be decipherable, since for every massing of human beings there would be a  corresponding massing of certain nematodes. Trees would  still stand in ghostly rows representing our streets and highways. The location of the various plants and animals would still be decipherable, and had we sufficient knowledge, in many cases even their species could be determined by an examination of their erstwhile nematode parasites." from "Nematodes and Their Relationships", 1915 Nathan Augustus Cobb, father of American nematology. Hydrostatic skeletons of NematodaPseudocoelom locomotionCFHCTA and adaptive volume of a fluid-filled cavity Nematodes Speciose: 20000 described More than a million to go. What is the most famous nematode and what is it most famous for? See next slide: C. elegans: for being the first animala whose genome was entirely sequenced.

9. Pseudocoelom as fluid skeleton Caenorhabditiselegans* • Phylum Nematoda Roundworms pinworms: most too small (<2mm) to leave any casual impression on laypeople. • Most free-living in soil; some parasitic. • Nematodes in the ocean? They are parasites of whales but are they in the sea floor? • Unsegmented, i.e., not metameric • Circular body in transverse section, pointed ends • HAS NO CIRCULAR MUSCLES, ONLY LONGITUDINAL. • Remarkably high internal pressure of pseudocoel fluid. Locomotes lying on Its side and thrashing Its body about. * Jon Eisenback

10. Uniformity of body design • Though the number of nematode species is so great, they are unusually uniform in body design. “characteristic features …are largely independent of size, of diet and of stage of development [of free-living or parasitic existence].” “…the elementary student may be forgiven …for thinking …there is only one nematode but that the model comes in different sizes and with a great variety of life histories. (Harris & Crofton 1957)”. (Flatworms and corals are much more diverse in morphology – so the uniformity of the nematode ‘body plan’ cannot be explained as because these worms are simpler organisms.) • A D’Arcy Thompson (the diagram of forces man) is associated with the idea that mechanical principles constrain form. “A bridge, a ship, an aeroplane are recognizable at once because their design is based necessarily and largely on the mechanical forces which play such a predominant part in their economy” (Harris & Crofton 1957). The features of an animal or plant available for evolution to act upon are limited or constrained by the mechanically possible. Natural selection constrains what evolves -- but so also do physical laws. • Nematode shape is dictated by mechanical considerations. Being an elongated unsegmented cylinder is key to its locomotion. Every soil-living nematode needs to have this pointed-end cylindrical in the middle shape.

11. Fluid skeleton locomotion with only one set of muscles: nematodes • More sources for fluid skeletons: • *Shadwick R.E. 2008. Foundations of animal hydraulics: geodesic fibres control the shape of soft bodied animals. J. exp. Biol. 211: 289-291. • Discussion of the importance of a classic paper: • Clark R.B., Cowey J.B. 1958. Factors controlling the change of shape of certain nemertean and turbellarian worms. J. exp. Biol. 731-748. • Harris J.E., Crofton H.D. 1957. Structure and Function in the nematodes: internal pressure and cuticular structure in Ascaris. J. exp. Biol. 34: 116-130. • *Assigned for reading. Just Shadwick, other references for background reading.

12. Worm as a fibre-reinforced cylinderClark-Cowey model “one of the key design principles of structural systems in biology” (Shadwick 2008) • From the 1950s the concept has existed of a hydrostatic skeleton: “a system in which muscles shorten to act against a contained volume of fluid, rather than rigid skeletal elements [sclerites, bones] to maintain shape and effect movement” (op. cit.) The important role of collagen helices is more recent and begins with Clark & Cowey. • “…a structure composed of inextensible fibres [can] accommodate large extensibility” is the basic idea of the Clark & Cowey paper (Shadwick 2008). • “…how [did a pseudocoelomate]… move if it had only one set of muscles as in the case of nematodes” (op. cit.) • “…the geometry of the reinforcing fibres in the body wall was the key to the solution…”. An antagonist of the longitudinal muscles of nematodes is a collagen fibre helix in the cuticle. • [ memonic device ‘CFHCTA’ Canadians For Happy Carefree TAs : crossed fibre helical connective tissue arrays (Kier).]

13. The Clark-Cowey model as explained by Kier, but see also Shadwick • A: imagine the worm as a fluid-filled cylinder one unit long, its wall stiffened by one turn of a collagen fibre helix. • There is a (helical) fibre angle ø: as the segment lengthens, cylinder diameter and ø both decrease [at 0° a thread]; as the segment shortens, its diameter and ø both increase [at 90° flat disc]. • If one plots the volume of the cylinder (y axis) vsfibre angle ø (x axis), V will vary following this curve, its cylindrical body remaining circular in transverse section. B represents the unit length of the worm cut along the top and laid open, D being the fibre length.

14. The Clark-Cowey model as explained by Kier, but see also Shadwick • So the area under the curve depicts volume change with ø change in a cylindrical worm. “A worm with a volume equal to the maximum that could be enclosed by the fiber system at [55°] would be unable to elongate or shorten significantly because any length change would entail a decrease in volume of an essentially incompressivle fluid…” Kier, p. 1249. • THE WORM CAN’T FOLLOW THE CURVE; it has to ‘pick’ a volume and live with it. Curve peaks at about 55°.

15. Clark-Cowey model Volume of the cylindrical fibre system changing with fibre angle. A worm is longer and thinner at lower angles (F) and shorter and fatter at higher angles (G). A worm species ‘chooses’ a constant volume, i.e., a horizontal line somewhere along the y axis e.g. FG. This gives the range over which its fibres can contribute to length change: for FG it is from 25 to ~82 helix inclination angle. `81. “The system can always contain less than this volume if the cross section becomes elliptical instead of circular. Allowing a worm to adopt a flattened elliptical cross-section as it changes length.“ Only where the horizontal line intersects the curve will the worm be circular in cross section. I don’t follow this, gkm.

16. The fluid cavity of a nematode can evolve to an adaptive range of extensibility that depends upon the relationship between the possible range of helical fibre angles and the fixed volume of the species. Pick a particular fixed volume (up the y axis) – a larger volume – and the range of helix angles available for shape change (involving flattening as the circular body goes to an elliptical cross section) is more constrained. More extensible species (e.g., Lineus) will evolve to use a volume that is giving the helix a greater range of angles.

17. In nematodes “…the body wall provides a passive elastic antagonist to muscle contraction, even though there are no elastic (i.e., stretchy) elements. Furthermore since the fibres are loaded in tension this sets up the possiblility of elastic energy storage to aid in the recoil and extension of the relaxing muscle.” (Shadwick 2008) I would have thought this is more than a possibility. The CFHCTA can act as antagonist to the return of the longitudinals to their precontracted state – at least in part – and the longitudinals on the left side can also stretch those of the right and vice versa. So helical collagen fibres can provide an antagonist to longitudinal muscles, and the volume of a nematode’s pseudocoel can be an adaptation for optimal extensibility. But the issue would seem still to be: how do nematodes actually move through the soil? How do they obtain purchase without chaetae? Is obtaining purchase an explanation for the pointed anterior and posterior body?

18. More attempts to understand the Clark-Cowey worm-volume curve • Suppose a nematode worm with a fixed volume of fluid skeleton and its helical collagen fibre array moving between 25 and 80˚. Over this range of angles the worm’s shape varies from longer and thinner at the ‘25-end’ to shorter and fatter at the ’80-end’. But the fluid cavity (pseudocoel) must stay the same volume over this range of angles [in a way the curve shape no longer matters, i.e., there is nothing special about 55˚as the high point] but the worm does lengthen or shorten via the helix, this involving flattening of its circular (section) shape to an ellipse. The worm’s helix can thus act as a means of affecting body shape in opposition to the longitudinal muscles. • The lengthening of the helix (via energy derived from the longitudinal muscles) can act to antagonize those muscles over a range of ‘extensibility’. • Where the worm species has ‘chosen’ its volume on the angle-volume curve can be adaptive or maladaptive depending on selection for better or worse extensibility.