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Phylogenomics and the evolution of Annelida

NSF-ATOL-1036537 “Collaborative Research: WormNet II: Assembling the Annelid Tree of Life”
DFG-STR-683/7-1 “AnnEvol – Evolution and phylogeny of Annelida based on phylogenomic data (i.e. EST libraries)”

Annelids are found throughout terrestrial, aquatic, and marine habitats, and are the most abundant component of the macrofauna in the deep sea. Traditionally, Annelida were thought to comprise "Polychaeta" and Clitellata as the highest ranked taxa (but see here). Polychaete annelids have been classified into over 80 "families", which are supported as monophyletic to greater or lesser degrees by morphological data. A recent and often used hypothesis of annelid relationships suggests a monophyletic "Polychaeta" consisting of two major clades, Scolecida and Palpata, the latter divided into Canalipalpata and Aciculata. However, their evolution is poorly understood and monophyly of all four major polychaete clades has been questioned. Furthermore, Clitellata is most likely a polychaete subtaxon rendering "Polychaeta" paraphyletic.

To test this hypothesis, multiple data sets have to be explored to evaluate the diversity and relationships of the major clades that comprise Annelida. A first phylogenomic data set comprising 231 genes significantly rejects all of the four clades, but provide convincing and significant support for major clades in the annelid phylogeny, which previous studies lacked. Chaetopteridae followed by Sipuncula and Myzostomida were sister to a clade comprising all other annelids, which split into two major clades, Errantia and Sedentaria (including Clitellata), reviving a 150-year-old neglected hypothesis. Ancestral character trait reconstructions revealed that Errantia are adapted to a more mobile and active life strategy due to increased sensory perception and motility and Sedentaria to a more sessile one with accompanying reductions of head and body appendages and position of the chaetae in closer proximity to the body wall.

Furthermore, already single gene analyses show some intriguing results concerning variability in annelid life history traits and morphological features. The transition from the marine habitat to the freshwater-terrestrial one occurred at least two times within Annelida (Clitellata, Parergodrilidae). Concerning the phylogeny of Eunicida and the evolution of their particular jaw apparatuses a surprisingly complex history was revealed contrary to previous analyses based on morphological characters of both recent and fossil jaw elements. Scaleless Pisionidae is part of the scale worms and holopelagic taxa are closely related to large, benthic annelids.

In the NSF-AToL project "WormNet II" and the DFG prject "AnnEvol" we, an international team of researchers, will address outstanding questions in annelid evolution at different taxonomic levels using a multi-tiered approach. We will establish EST databases using high-throughput sequencing technologies for up to 250 annelid species as well as 10 nuclear genes for up to 400 taxa. This research regarding the evolution of annelids in general as well as of subtaxa at the order or family level will accompanied by a community sequencing approach of mitochondrial markers to address outstanding questions at the genus and species level. Hence, we will gain insights into different  aspects of annelid evolution within annelids, but also with respect to other lophotrochozoan taxa.

 
 
Fig. 1. Bayesian analyses were performed on the basis of 47,953 amino acid positions derived from 231 genes. Posterior probailities (upper value or alone) and bootstrap support (lower value) values ≥ 0.70 or 70, respectively, are shown at the nodes. The tree is from Struck et al. (2011).



Fig. 2. Depictions of the ancestral reconstructions of body and parapodial characters for (a) Annelida and clade 1, (b) Errantia, and (c) Sedentaria. The state of several parapodial characters in (a) Annelida and clade 1 is uncertain, and therefore we depicted the two most extreme possibilities. Dashed drawings or ? indicate that the state of this character is uncertain.  Modified from Struck et al. (2011).

* Struck, T. H., Paul, C., Hill, N., Hartmann, S., Hösel, C., Kube, M., Lieb, B., Meyer, A., Tiedemann, R., Purschke, G. & Bleidorn, C. (2011). Phylogenomic analyses unravel annelid evolution. Nature. 471: 95-98.
* Struck, T. H. & Halanych, K. M. (2010). Origins of holopelagic Typhloscolecidae and Lopadorhynchidae within Phyllodocidae (Phyllodocida, Annelida). Zoologica Scripta 39: 269–275.
* Zanol, J., Halanych, K. H., Struck, T. H. & Fauchald, K. (2010). Phylogeny of the bristle worm family Eunicidae (Eunicida, Annelida) and the phylogenetic utility of noncongruent 16S, COI and 18S in combined analyses. Molecular Phylogenetics and Evolution 55: 660-676.  
* Struck, T. H., Nesnidal, M. P., Purschke, G. & Halanych, K. M. (2008). Detecting Possibly Saturated Positions in 18S and 28S Sequences and their Influence on Phylogenetic Reconstruction of Annelida (Lophotrochozoa). Molecular Phylogenetics and Evolution 48: 628–645.
* Zhong, M., Struck, T. H. & Halanych, K. M. (2008). Phylogenetic information from three mitochondrial genomes of Terebelliformia (Annelida) worms and duplication of the methionine tRNA. Gene 416: 11–21.
* Halanych, K. M., Cox, L. N. & Struck, T. H. (2007). A brief review of holopelagic annelids. Integrative and Comparative Biology 47: 872-879.
* Struck, T. H., Schult, N., Kusen, T., Hickman, E., Bleidorn, C., McHugh, D. & Halanych, K. M. (2007). Annelida phylogeny and the status of Sipuncula and Echiura. BMC Evolutionary Biology 7:57.
* Struck, T. H., Purschke, G. & Halanych, K. M. (2006). Phylogeny of Eunicida (Annelida) and Exploring Data Congruence using a Partition Addition Bootstrap Alteration (PABA) approach. Systematic Biology 55: 1-20.
* Struck, T. H., Purschke, G. & Halanych, K. M. (2005). A scaleless scale worm: Molecular evidence for the phylogenetic placement of Pisione remota (Pisionidae, Annelida). Marine Biology Research 1: 243-253.
* Struck, T. H. & Purschke, G. (2005). The sister group relationship of Aeolosomatidae and Potamodrilidae (Annelida: “Polychaeta”) – a molecular phylogenetic approach based on 18S rDNA and cytochrome oxidase I. Zoologischer Anzeiger 243: 281-293.
* Burnette, A. B., Struck, T. H. & Halanych, K. M. (2005). Holopelagic Poeobius meseres (“Poeobiidae,” Annelida) Is Derived From Benthic Flabelligerid Worms. Biological Bulletin 208: 213-220.
* Jördens, J., Struck, T. H. & Purschke, G. (2004). Phylogenetic inference regarding Parergodrilidae and Hrabeiella periglandulata (‘Polychaeta’, Annelida) based on 18S rDNA, 28S rDNA and COI sequences. Journal of Zoological Systematics and Evolutionary Research 42: 270-280.
* Struck, T. H., Hessling, R. & Purschke, G. (2002). The phylogenetic position of the Aeolosomatidae and Parergodrilidae, two enigmatic oligochaete-like taxa of the ‘Polychaeta’, based on molecular data from 18S rDNA sequences. Journal of Zoological Systematics and Evolutionary Research 40: 155-163.

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