Self-organizing animals.

In earlier posts I introduced bryozoans: filter feeding invertebrates that grow by budding to form groups of interconnected clones. One of my favorite things about bryozoans is that some of them self-organize to form structures much larger than the individual animal (unless you count the whole colony as the individual animal). My favorites (Membranipora sp.) grow as big sheet-like colonies covering surfaces. Most individuals stick their crowns of tentacles out out of their coffin-shaped boxes to form a canopy over the surface of the colony. They each pump water through themselves to feed on tiny planktonic organisms. The water has to have somewhere to go or else they wouldn't be able to keep feeding. Certain patches grow taller than their neighbors, and lean to the side to make openings in the canopy (also, individuals in the center of these patches often degenerate). The water squirts out of these chimney-like openings at relatively high speeds, so it gets mixed farther from the colony, and the individuals don't keep re-filtering the same water.

The resulting form and water flow patterns are beautiful. The first image here shows what a ~3cm wide colony looks like from the top; the second image shows a different colony from the side. I used a sheet of light to illuminate just a single slice through the chimney in the second image. Colorizing each frame differently makes the flow stand out: moving particles appear as rainbows, while the still tentacles appear white.

The really cool parts about the chimneys that the colony organizes the chimneys based on information in the water flow that the chimneys control: the colony forms chimneys at the growing edge of the colony where the water flows out fastest [1], and can be induced to form new chimneys by manipulating the flow [2]. This feedback between water flow and form appears to allow them to respond to all sorts of perturbations that affect the water flow: injuries from predators, the formation of spines to defend against predators, variation in the form of the surface they grow on, etc [3].

This same kind of feedback between flow and form shows up in our blood vessels [4, 5], the gut/circulatory canals of hydroid colonies [6, 7], the veins of giant unicellular slime molds [8]. These systems evolved independently, serve different functions, and have very different structures, yet are united by the physics of moving fluids [9].

1. von Dassow, M., Flow and conduit formation in the external fluid-transport system of a suspension feeder. Journal of Experimental Biology, 2005. 208(15): p. 2931-2938 DOI: 10.1242/jeb.01738.
2. von Dassow, M., Function-dependent development in a colonial animal. The Biological Bulletin, 2006. 211(1): p. 76-82 DOI: 10.2307/4134580.
3. Grunbaum, D., Hydromechanical mechanisms of colony organization and cost of defense in an encrusting bryozoan, membranipora membranacea. Limnology and Oceanography, 1997. 42(4): p. 741-752.
4. Kamiya, A. and T. Togawa, Adaptive regulation of wall shear-stress to flow change in the canine carotid-artery. American Journal of Physiology - Heart and Circulatory Physiology 1980. 239(1): p. H14-H21.
5. Langille, B.L., Blood flow-induced remodeling of the artery wall, in Flow-dependent regulation of vascular function, J.A. Bevan, G. Kaley, and G.M. Rubanyi, Editors. 1995, Oxford University Press: New York, N.Y. p. 277-299.
6. Buss, L.W., Growth by intussusception in hydractiniid hydroids, in Evolutionary patterns: Growth, form, and tempo in the fossil record, J.B.C. Jackson, S. Lidgard, and F.K. Mckinney, Editors. 2001, University of Chicago Press: Chicago. p. 3-26.
7. Dudgeon, S.R. and L.W. Buss, Growing with the flow: On the maintenance and malleability of colony form in the hydroid hydractinia. American Naturalist, 1996. 147(5): p. 667-691.
8. Nakagaki, T., H. Yamada, and T. Ueda, Interaction between cell shape and contraction pattern in the physarum plasmodium. Biophysical Chemistry, 2000. 84(3): p. 195-204 DOI: 10.1016/S0301-4622(00)00108-3.
9. Labarbera, M., Principles of design of fluid transport-systems in zoology. Science, 1990. 249(4972): p. 992-1000.

Re-building a whole new body

Imagine how handy it would be if you could rebuild your whole body from a tiny fragment. Some animals can do this, but most such animals (e.g. sponges, hydra, and planarians) have elegantly simple internal structure. But it turns out that many botryllid ascidians, among our closest living invertebrate relatives, are also able to do this [1-3]. As mentioned in a previous post, these marine animals have the same basic organization that we do: each individual has a heart, central nervous system, and through-gut, as well as a number of other features shared with vertebrates.

Adult botryllid ascidians can reproduce sexually, with eggs that develop in a precisely choreographed manner to form a swimming larva. The larva metamorphoses into the founding member of a colony of interconnected individuals that live attached to surface. Each individual reproduces asexually by forming buds as pouches off the tissues surrounding its heart. But under certain conditions (which vary by species [1-3]) the colony can form a whole new individual from aggregates of blood cells. Circulating cells clump up on the wall of one of the blood vessels that reach to the outer edge of the colony [1]. Then the clump hollows out, and starts to mold itself into a new body from scratch*. Because these organisms are fairly closely related to humans, this process likely holds insights for regenerative medicine [3].

However, what I find most exciting is that it shows that development can tolerate remarkable variation. Developmental biology tends to focus on the complicated interplay of interactions required in "normal" development from the egg. We usually think of development as fragile, easily thrown off by a mutation here, or a sip of wine there. But this example dramatically shows that – at least in a few organisms surprisingly closely related to ourselves – cells can organize themselves into the same body from lots of different starting points. Botryllids can form complete new individuals in at least three very different ways: a precise series of events from egg to larva to juvenile; from pouches of a specific epithelium; or from disorganized aggregates of blood cells. Understanding how they do this could reshape how we think about animal development.

*The outer epithelium apparently comes from the cells lining the outside of the blood vessel. Their blood vessels do not have the inner lining of cells that our vessels have.

1) The clearest images and diagrams of this process come from the first description, which is freely available online: Oka, H., and Watanabe, H. 1957. Vascular budding, a new type of budding in Botryllus. Biological Bulletin 112:225–240.
2) This has some neat videos, and some interesting results about the importance of maintaining blood flow for regeneration. Voskoboynik A, Simon-Blecher N, Soen Y, Rinkevich B, De Tomaso AW, Ishizuka KJ, Weissman IL. 2007. Striving for normality: whole body regeneration through a series of abnormal generations. The FASEB Journal 21:1335–1344.
3) This one also has neat videos and discusses the some of the possible molecular pathways involved. Brown, F.D., Keeling, E.L., Le, A.D., and Swalla, B.J. 2009. Whole Body Regeneration in a Colonial Ascidian, Botrylloides violaceus. Journal of Experimental Zoology (Mol. Dev. Evol.) 312B:885-900