Water bears & velvet worms: Georg Mayer on neural clues to panarthropod evolution

Posted by Biome on 23rd December 2013 - 0 Comments


When it comes to the phylogenetic tree of life the specific branch on which the microorganisms tardigrades hang is a point of controversy. These extremophiles, also known as water bears, have been regarded as a sister group to arthropods, onychophorans (also known as velvet worms), onychophorans plus arthropods, and even nematodes. Both molecular and morphological approaches to phylogenetic analysis have not provided a clear consensus on where tardigrades fit. Although they show similarities to existing onychophorans in having unjointed limbs, their nervous system shows a segmental organisation resembling that of arthropods. In a recent study published in BMC Evolutionary Biology, Georg Mayer from the University of Leipzig, Germany, and colleagues explore the neuroanatomy of tardigrades to clarify the phylogenetic position of this enigmatic animal group. Mayer tells us more about why there has been such uncertainty over their evolution and how their findings help bring some clarity to this conundrum.

 

Scanning electron micrograph of an adult tardigrade. Image source: Wikimedia, Goldstein

What is a tardigrade and why are they so controversial in terms of their evolution?

Tardigrades or water bears are tiny invertebrates, typically not exceeding one millimetre in length, that inhabit many parts of our planet, including the deep sea, the highest mountains, and Antarctica. Some tardigrades are known for their remarkable survivability, as they are able to tolerate total desiccation, freezing temperatures and high radiation levels. They even survived – unassisted – when exposed to outer space, which is unique for multicellular organisms. The mechanisms that enable them to withstand these extreme conditions are poorly understood.

Tardigrades are also enigmatic in terms of evolution because zoologists do not know exactly where to place these animals in the tree of life. They might be closely related to arthropods, onychophorans (velvet worms), Cambrian lobopodians or nematodes, but their precise relationship to one of these animal groups is controversial.

The tardigrade genome is rather small, probably due to extensive gene loss, and most gene sequences show high substitution rates. This causes problems with phylogenetic reconstructions using molecular datasets, due to the so-called Long Branch Attraction artefact. This means that taxa with a high substitution rate artificially cluster together. Most morphological data seem to be equally problematic, as key characteristics might have been lost due to the miniaturisation of these animals and the remaining characteristics might be highly derived. Hence their origin is difficult to interpret.

 

Alternative hypotheses on the phylogenetic position of Tardigrada within the superphylum Ecdysozoa. Image source: Mayer et al, BMC Evolutionary Biology, 2013, 13:230

What interested you in the tardigrade nervous system in particular?

Speaking more generally, nervous systems have the advantage that their structure seems to be more conserved than that of any other organ system, possibly due to functional or developmental constraints. Zoological literature is full of examples illustrating that the animal’s body plan usually changes faster than the architecture of its nervous system. Hence, analysing the neuroanatomy of an animal might provide important insights into the changes that have taken place during evolution. Another advantage of neuroanatomical studies is that neural structures can be selectively labelled with specific markers and efficiently analysed using new powerful imaging techniques, such as confocal laser-scanning microscopy. Provided these methods work, they help generate a large amount of useful data within a relatively short period of time.

It was previously known that tardigrades have segmental ganglia [groups of nerve cells located outside the brain that are segmentally repeated and connected along the body], but the relationship of these structures to the segmental ganglia that are characteristic of arthropods was uncertain. Some authors had even claimed that segmental ganglia evolved independently in tardigrades and arthropods. In fact, there are numerous other uncertainties and controversies. For example, while a very early study using light microscopy in 1840 revealed that tardigrades possess unusual extra-ganglionic commissures between the paired connectives that join their ganglia, their existence was doubted by subsequent authors. Hence, we decided the time was ripe for an in-depth investigation of the tardigrade nervous system using state of the art anatomical techniques.

 

What are the main new findings that your study reveals and how do they relate to arthropods and onychophorans?

Our study revealed striking similarities in the basic architecture and position of segmental ganglia in tardigrades and arthropods. These findings speak against the proposed sister group relationship of tardigrades with nematodes. They suggest instead that Tardigrada and Arthropoda are sister groups (to the exclusion of Onychophora). Moreover, our findings clearly refute a previous hypothesis, according to which there are no contralateral connections linking the hemiganglia of each body side. From the functional perspective alone, this hypothesis was unlikely to be correct, as it suggested that there was no neural coordination between the two body sides. However, if one looks at a living tardigrade, one can clearly see that the leg movements of each body side are perfectly coordinated, implying the presence of neural pathways linking the two body sides. Our study now clearly shows that there are indeed numerous contralateral projections in each trunk ganglion. Furthermore, we confirmed the existence of additional, extra-ganglionic commissures. We interpret them as remnants of an ancient set of interpedal commissures in the last common ancestor of Panarthropoda (arthropods plus tardigrades plus onychophorans).

 

What is your position on the molecules versus morphology debate in the identification of species?

Although our study on the tardigrade nervous system might sound ‘pro morphology’ and ‘contra molecules’, this is not our general attitude. We typically apply both morphological and molecular methods for our research, in particular for species descriptions (see our website on Onychophora). I am not confined to a particular method, as no single technique can be regarded as superior to the exclusion of others. What really matters is the scientific question one wants to answer. In my view, if one really wants to resolve a particular question, then you have to be open to acquiring the required skill. Luckily, there are lots of experts out there who can usually help out.

 

What are the next steps for your research?

Together with my team, I am trying to broaden our methodological spectrum to get further insights into the evolutionary history and development of onychophorans, tardigrades and arthropods. Despite the challenges, working with these animals is fascinating because it allows us to look back hundreds of millions of years to the time when these animal lineages had diverged from each other.

 

Questions from Elizabeth Moylan, Biology Editor for BioMed Central.

 

More about the author(s)

Georg Mayer, Group leader, University of Leipzig, Germany.

Georg Mayer obtained his PhD from the Free University of Berlin, Germany, and went on to receive several research fellowships funded by the German Research Foundation. In 2010, Mayer established his laboratory at the University of Leipzig, Germany. Research in the Mayer lab focuses on understanding the evolution of arthropod diversity by studying their closest relatives, onychophorans (velvet worms) and tardigrades (water bears). By analysing their anatomy, development, phylogeny and other aspects the Mayer lab aims to uncover the evolutionary changes that have taken place since these animals diverged from arthropods.

Research article

Selective neuronal staining in tardigrades and onychophorans provides insights into the evolution of segmental ganglia in panarthropods

Mayer G, Martin C, Rüdiger J, Kauschke S, Stevenson PA, Poprawa I, Hohberg K, Schill RO et al.
BMC Evolutionary Biology 2013, 13:230

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