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Leggy creatures and long branches

Tracking centipedes and millipedes to their exact location in the evolutionary tree.

Centipedes and millipedes have often been neglected in studies of arthropod relatedness. Credit: Emanuele Biggi / OSF / Photolibrary

Biologists have amassed further ammunition in the debate over the position of centipedes and millipedes among their spider, insect and crustacean kin. They've positioned the many-legged group alongside insects and crustaceans, a finding that could put warring zoologists at ease.

In a report published today in Proceedings of the Royal Society B1, the authors report the first use of microRNA as a genetic marker to clarify relationships among arthropods — creatures like crabs, cockroaches and centipedes, with jointed legs — and offer analyses that counter previous hypotheses.

The arthropod family is immense, accounting for more than 80% of all known animals and encompassing insects, crustaceans, spiders and Myriapoda — centipedes and millipedes. Myriapods have been neglected and frequently relocated in studies of arthropod relationships.

In the late nineteenth century, zoologists believed myriapods to be ancestral arthropods because they looked like earthworms with legs. Soon this hypothesis gave way to one that had myriapods nestling next to insects, sharing a hypothetical air-breathing ancestor. With the advent of DNA sequencing, crustaceans and insects were bracketed together, and the position of centipedes and millipedes has been contentious ever since.

Enter Mandibulata

Head structures have emerged as a key criterion in organizing the unruly arthropod family. Because myriapods, insects and crustaceans have similarly segmented heads, mouth parts and mandibles, morphologists today place the three groups together in a clade termed Mandibulata. Yet molecular phylogenies often refute the existence of Mandibulata, instead positioning myriapods beside spiders, scorpions and horseshoe crabs in a clade so perplexing that it has been termed Paradoxopoda (or Myriochelata).

If the Paradoxopoda arrangement is correct, the intricate heads and mandibles of myriapods, crustaceans and insects must have evolved multiple times independently — or otherwise been lost without leaving a trace in spiders and their kin. This is not impossible, but it is implausible, says Max Telford of University College London, an author on the paper, which favours Mandibulata. His team's work might have broken Paradoxopoda's last leg.

"This paper is absolutely a relief to morphologists because it is thoroughly convincing and includes a lot of data coming in from different angles," comments Graham Budd at Uppsala University in Sweden, who was not involved in the study.

Molecular data on arthropoda have delivered surprises in the past that eventually gained widespread support. Insects and crustaceans were united based on sequence data, for example, and the group is now widely accepted because the creatures share other characteristics as well. Paradoxopoda, however, has gained little support. Yet the debate has continued to rage. So Telford and his team undertook a last-ditch effort to get to the bottom of the Mandibulata mystery.

Spiders out

Using microRNA to trace evolutionary relationships, the team found a common sequence in crustaceans, centipedes and millipedes that did not appear in spiders, horseshoe crabs or ticks, raising support for Mandibulata.

"MicroRNAs tend to be very precise as phylogenetic markers because they are rarely lost and they evolve very slowly," explains co-author Davide Pisani at the National University of Ireland in Maynooth. Phylogenetic analyses of new morphological characteristics and protein-coding genes supported the Mandibulata as well, lending credence to earlier studies2,3 that came to the same conclusions by analysing different sets of genes.

Telford's team went on to explore why some other studies had failed to find Mandibulata. "Why did Dunn et al. get bits of their tree wrong?" Telford asks, citing a phylogeny that supports Paradoxopoda4. After running various tests, the team concluded that Paradoxopoda came about, in part, as a result of 'long branch attraction', a misleading effect caused by the way in which data are analysed. The effect pulls together rapidly evolving lineages, regardless of their evolutionary relationship.

Long branch attraction might be pulling the insects and crustaceans, each with fast-evolving genes, close together and towards groups outside the arthropods, stranding the slowly evolving myriapods with the chelicerates, says Telford. When the researchers excluded quickly evolving genes or quickly evolving species, support for Mandibulata increased. They performed the same procedure on data from the paper of Dunn et al., with similar results.

With their enormous diversity, and a history dating back more than 520 million years, the arthropods push phylogeneticists to the limit. The clade of the Mandibulata may finally be accepted, says Telford. But other nodes — such as the position of insects relative to crustaceans, of sea spiders relative to spiders, and of water bears and velvet worms relative to arthropods — remain contentious.

Other regions of the animal tree might make for smoother sailing, but where's the skill in that? Telford says, "If we make a tree and horses and zebras go together, it could be for all the wrong reasons. But who cares — we'll never know that our model doesn't work."

References

  1. Rota-Stabelli, O. et al. Proc. R. Soc. B doi:10.1098/rspb.2010.0590 (2010).

  2. Regier, J. C. et al. Nature 463, 1079-1083 (2010).

  3. Giribet, G., Edgecombe, G. D. & Wheeler, W. C. Nature 413, 157-161 (2001).

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  4. Dunn, C. W. et al. Nature 452, 745-749 (2008).

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Nature, Arthropod phylogeny

Nature, Animal phylogeny

Nature, Review of Arthropod evolution

Nature Letter, Broad phylogenomic sampling improves resolution of the animal tree of life

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Maxmen, A. Leggy creatures and long branches. Nature (2010). https://doi.org/10.1038/news.2010.397

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