How siphonophores grow

In this new animation from our series creaturecast.org, Riley Thompson describes how siphonophores grow.

The midwater is the part of the ocean that is below the surface and above the bottom. The midwater is big — it makes up well over ninety percent of the space that life inhabits on Earth. Even so, this is an environment that is very foreign to humans. The only midwater animals we regularly encounter are those that have hard skeletons, like fish and crustaceans, that are sturdy enough to be plucked intact from the midwater with nets or hooks. They provide a very biased view of what lives in the ocean midwater.

Many other groups of animals have independently come to live permanently in the midwater, including snails, medusae, and comb jellies. The midwater is pitch black and cold. The animals that live in the midwater have nothing to walk on, burrow in, or attach themselves to. They have nowhere to hide. The effect of gravity on these animals is relatively weak, because most are neutrally buoyant. They don’t need to invest in structural elements like rigid skeletons because they do not experience the turbulence of the surf, the swell at the surface, or of the currents that can sweep across the ocean bottom. All of these environmentel features lead to the repeated evolution of animals that are gelatinous, clear, and extremely fragile. This is why so many different animals have independently converged on similar “jellyfish” features.

Siphonophores are one of the most abundant, and also one of the most poorly known, of the large midwater animals. There are 175 described species of siphonophores, though only one is regularly encountered. This is the Portuguese Man o’ War, which floats at the surface and is propelled by the wind as it drags its tentacles through the water. It is best known for its powerful sting.

Portuguese man o’ war floating at the surface.

Most other siphonophores live exclusively in the midwater and are beautiful, elongate animals that resemble a Chihuly chandelier that has come to life. While some are only a few centimeters long, others reach lengths of more than 30 meters. Siphonophores are predators that set a web of tentacles that ambush prey, like a giant underwater spider web, or lure fish to them with light and motion.

Siphonophores can seem alien to humans. Direct comparisons to our own biology turn up some striking differences, and help us to understand the biology of familiar animals, including ourselves, within a broader context. Take the division of labor in our body. Humans perform many different complex tasks to survive, and these tasks are distributed across specialized parts of our bodies. Key metabolic tasks are centralized to our liver, our muscles move our whole body (including the non-muscular bits that would otherwise be immobile), and food is broken down in our digestive organs. Like the division of labor in economies, this division of labor within our bodies improves efficiency and enables activities that wouldn’t be possible without specialization. Understanding the evolution of the division of labor is central to understanding the evolutionary origins of biological complexity.

The type of division of labor that we have — where we each have one body with specialized parts — seems so ordinary only because it is so familiar. There are other ways to be an organism with many complex, specialized parts. Siphonophores are a prime example. Like corals and some other animals, siphonophores are colonial. Instead of growing by enlarging their body, they just clone themselves and add many smaller bodies. The bodies stay attached to each other, and have connected circulatory systems that share resources among them. This sharing means that not all bodies need to eat, and they can dedicate themselves to other tasks such as swimming and sexual reproduction of new colonies.

Specialized bodies of the siphonophore Nanomia bijuga. From the animation at https://vimeo.com/114198648.

We know each siphonophore is made up of many multicellular bodies rather than many organs because we can still see the parts of the bodies that are found in solitary, non-colonial bodies. It is as if you were born as a normal human baby, but then instead of getting larger you began budding new attached twins each specialized for particular tasks such as feeding, walking, defense, and sex.

Among colonial animals, the division of labor in siphonophores is taken to an extreme — there can be more than ten types of specialized bodies, and these bodies are arranged in precise, species-specific patterns. All the bodies within a siphonophore colony are genetically identical because they bud from a single embryo. Bodies don’t fuse to form a siphonophore colony.

Because they are so fragile and difficult to collect, there has been little research on the organization of bodies within siphonophore colonies or on how new bodies are added as they grow. My lab at Brown University works on these questions. We collect intact siphonophores by remotely operated underwater vehicles with our collaborator Steve Haddock at the Monterey Bay Aquarium Research Institute, by SCUBA diving from ships in the open ocean, and by dipping siphonophores from the surface where they come close to shore.

Siphonophores have growth zones where they elongate and new bodies are added. Our first order of business was to describe the budding process that gives rise to these new bodies within these growth zones. We found that the budding process in many siphonophores gives rise to clusters of bodies that then spread out along the rope-like stem. This is the case in Nanomia bijuga, the siphonophore whose growth we have examined in the greatest detail and that is animated in this episode of CreatureCast.

The budding process that leads to siphonophore growth. Green indicates feeding bodies, and purble indicates digestive bodies (palpons). Excerpted from https://vimeo.com/114198648.

Once we knew the general features of the budding process, the next questions were about the cellular processes (including cell division and differentiation) that produce this budding. Stefan Siebert, a postdoctoral researcher, found that siphonophore stem cells are located only at very specific regions in the colony. They are concentrated in the growth zones, budding bodies, and specific sites within some mature bodies. As each body grows, its stem cells become more restricted.

The distribution of stem cell gene expression (blue, green, and yellow) and cell proliferation (magenta) in the siphonophore Nanomia bijuga. See the caption of the original figure for more details. http://evodevojournal.biomedcentral.com/articles/10.1186/s13227-015-0018-2#Fig8

This suggests a new explanation for the precise, complex growth and form of siphonophores. Because stem cells are not widespread and do not seem to migrate, as in many other colonial animals, the addition of new bodies is restricted to particular sites — the growth zones. This restriction in turn may allow for a very regular and precise placement of new bodies of many different types.

In parallel, we have worked to describe how the specialized bodies differ from each other. Stefan identified genes that differ in activity between bodies. Sam Church, a former undergraduate student in the lab, described which cells are found in which bodies. Cat Munro, a graduate student in the lab, is currently working to see how differences in the activity of genes in siphonophore bodies change through the course of both development and evolution.

This episode of CreatureCast was created by Riley Thompson, based on a script that we wrote together. The animation is based in part on illustrations by Freya Goetz. More animations can be found at creaturecast.org, a project supported in part by the National Science Foundation.