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

Ascidian colonies

Erica Westerman (first author on the study discussed in my last post) kindly sent me two nice images of ascidian colonies*. The first image shows a pair of small Botrylloides violaceus colonies (orange) growing up to each other at the top of the image. The lower colony is getting overgrown by a larger colony of Botryllus schlosseri at the bottom (brown). The individual zooids within the colony are orange (or brown) oblongs set in rosettes of 6 or more. Each set of individuals sucks in water through an opening at the colony surface, and the water flows to an opening at the center of the rosette, shared by all the zooids in the rosette.

The second image shows several larger colonies, of Botrylloides violaceus growing into each other on a settling plate. You can still see the boundaries between the colonies, which are distinct in coloration, and the arrangement of zooids.

*As always, please do not use images without permission from the contributor.

Are you feeling like yourself today?

What it would be like if the people you lived with could take over your body? This is a (somewhat creepy) reality for a few of our closest invertebrate relatives, the botryllid ascidians.

Adult ascidians look nothing like vertebrates, but developmental and molecular similarities indicate they are close kin to vertebrates [1]. Adult ascidians live attached to a surface and filter food from the surrounding water. Some ascidians are colonial: they bud asexually to form an array of individuals that each have their own organs but share a common blood system.

At least one type of colonial ascidians – the botryllids – takes this a giant step further. When neighboring colonies meet they can fuse together so that both colonies share their blood, transmitting cells among the colonies [2-3]. Colonies only fuse if they share a particular version (allele) of one gene. If they don't share that allele, one colony may grow over the other, smothering it, or they may sit quietly side by side. However, in laboratory studies colony fusion leads to an unpleasant outcome for one of the colonies. One colony can take over the other, replacing the tissues of the second colony with its own cells*. Certainly a creepy way to die!

But what happens in the wild? To address this question, Erica L. Westerman et al. (2009) set out clean plates in Salem Harbor (MA) for larvae of one species, Botrylloides violaceus, to settle on [3]. The researchers monitored colony-colony contacts over several weeks. Surprisingly, almost all of the colonies fused! This is remarkable, given what has been observed under controlled conditions. Westerman et al. (2009) provide a very interesting and accessible discussion of factors that may differ between the lab and field, and of some of the possible advantages to fusing despite the risk of takeover.

Colony-colony fusion gives a fascinating window into the biology of individuality since all organisms, including ourselves, have to deal with the problem of how to tell what's part of themselves and what's not. And it remains an issue even for vertebrates: in a few mammals with low genetic diversity (e.g. dogs [4] and Tasmanian devils [5]), cancers have arisen that can spread among individuals since so many individuals share the same versions of the genes that distinguish self from non-self**. (This is not a problem for humans because our species has a high level of diversity in those genes). Hence, the peculiarities of the botryllids shed light on one of the most fundamental and challenging biological questions: what is an individual?

*It gets yet stranger since the second colony doesn't always lose out entirely. Sometimes the apparent loser takes over all the reproductive cells and becomes the sole parent of the next generation [2].
**Curiously, different animals use different genes to distinguish self from non-self.

1) Pechenik, J.A. (2000) Biology of the Invertebrates, 4th edition.
2) Rinkevich, B. (2005) Natural chimerism in colonial urochordates. Journal of Experimental Marine Biology and Ecology 322:93-109
3) Westerman, E.L., Dijkstra, J.A., and Harris, L.G. ( 2009) High natural fusion rates in a botryllid ascidian. Marine Biology 156:2613-2619
4) Rebbeck, C.A., Thomas, R., Breen, M., Leroi, A.M., and Burt, A. (2009) Origins and evolution of a transmissible cancer. Evolution 63(9): 2340–2349
5) Murchison, E.P. et al. (2010) The tasmanian devil transcriptome reveals schwann cell origins of a clonally transmissible cancer. Science 327:84-87