Phylogenetic position of interstitial polychaete taxa of supposedly paedomorphic origin using mitogenomic data
Final Report Abstract
Resolving the phylogeny of Annelida has always been challenging using either morphological or molecular data, especially with respect to several interstitial taxa (i.e., Dinophilidae, Apharyngtus punicus, Diurodrilidae, Protodrilidae, Protodriloidae, Saccocirridae, Polygordiidae, and Nerillidae). Using morphological data different alternative hypotheses regarding their placement within Annelida had been put forward, but support for these relationships was low. Moreover, regarding the origin of these taxa different evolutionary scenarios had been considered. The first was that these taxa showed the condition of the last common ancestor of Annelida (Archiannelida hypothesis). Another scenario proposed that at least some of these taxa evolved by paedomorphosis. That is, larval or juvenile stages of larger annelids, which temporarily inhabit the interstitium, became sexual mature and arrested in their further somatic development and, thus, permanently inhabited the interstitium. Yet another scenario was the gradual and step-by-step decrease in body size and reduction of certain features such as parapodia, also known as miniaturization. In this project we determined the mitochondrial genomes of 29 annelid taxa including 8 interstitial ones. The first outcome of this project was that the determination of mitochondrial genomes in nonmodel groups like Annelida is most efficiently accomplished using next-generation sequencing technology. In comparison to the classical strategy the shot-gun approach was considerably faster and less expensive. Using mitochondrial data we could show that the recent claim of a non-annelid affinity of Diurodrilidae has to be rejected as both mitochondrial sequence and gene order data strongly support the traditional hypothesis of an annelid affiliation. Moreover, both mitochondrial sequence and gene order data strongly support the monophyly of Protodrilida (Protodriloidae, Protodrilidae, Saccocirridae). All other hypotheses regarding the placement of the interstitial taxa based on morphological data were not supported. However, the power to resolve annelid phylogeny and the position of the interstitial taxa within Annelida in particular was low considering nodal support, but consistent placement of these taxa was generally achieved in thorough sensitivity analyses providing support to the placement of these taxa. First, Protodrilida and Polygordiidae were monophyletic and were the sister group of the errant annelids within Pleistoannelida. Second, Dinophilidae, Diurodrilidae, Nerillidae and Apharyngtus punicus, which were usually considered to be closely related to Errantia, were now placed within a larger sedentarian clade, that also comprised Parergodrilidae and Orbiniidae. Hence, with respect to the colonization of the interstitial realm and the evolutionary origin of these taxa the results based on the mitochondrial data tentatively substantiate two conclusions. First, the grouping of Dinophilidae, Diurodrilidae and Apharyngtus punicus together with Parergodrilidae and Orbiniidae suggests that these interstitial taxa permanently colonized the interstitium by paedomorphic evolution from an orbiniid-like ancestor. Their organization resembles a polytroch larvae, which can also be found in Orbiniidae. Moreover, these three taxa and Parergodrilidae as well as developmental stages of Orbiniidae possess a peristomium with two rings. The close relationship of Polygordiidae and Protodrilida to errant annelids argues against a paedomorphic origin of these taxa. In contrast, their organization can easily be derived from the recently suggested ground pattern of Annelida by reductions and losses of parapodia. Hence, Polygordiidae and Protodrilida more likely occupied the interstitium via a stepwise miniaturization of a larger ancestor and simplification by reductions. In conclusion, the adaptation of the annelids to the interstitium was not exclusively achieved by one evolutionary process, but at least by two different ones, paedomorphosis and miniaturization. Finally, the different studies in this project covering Annelida, Deuterostomia and Bilateria showed that the potential of mitochondrial genomes to resolve phylogenetic questions strictly depends on its molecular evolution. The phylogenetic study based on mitochondrial data (be it sequence or gene order data) is often hampered by biases such as branch length heterogeneity, base composition heterogeneity or strongly deviating gene orders. In these cases, as the mitochondrial genome can be regarded as one heritable unit all mitochondrial genes are usually affected by the biases. Thus, special care has to be taken in phylogenetic analyses of mitochondrial genomes and genes to minimize the impact of such biases on the reconstruction.
Publications
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(2011). Detecting the symplesiomorphy trap: A multigene phylogenetic analysis for terebelliform annelids. BMC Evolutionary Biology 11: 369
Zhong, M., Hansen, B., Nesnidal, M., Golombek, A., Halanych, K. M. & Struck, T. H.
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(2013). A comprehensive analysis of metazoan mitochondrial genomes and animal phylogeny. Molecular Phylogenetics and Evolution 69: 352-364
Bernt, M., Bleidorn, C., Braband, A., Dambach, J., Donath, A., Fritzsch, G., Golombek, A., Hadrys, H., Jühling, F., Meusemann, K., Middendorf, M., Misof, B., Perseke, M., Podsiadlowski, L., von Reumont, B., Schierwater, B., Schlegel, M., Schrödl, M., Simon, S., Stadler, P. F., Stöger, I. & Struck, T. H.
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(2013). Mitochondrial genomes to the rescue – Diurodrilidae in the myzostomid trap. Molecular Phylogenetics and Evolution 68: 312–326
Golombek, A., Tobergte, S., Nesnidal, M. P., Purschke, G. & Struck, T. H.
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(2013). The Impact of Mitochondrial Genome Analyses on the Understanding of Deuterostome Phylogeny. Molecular Phylogenetics and Evolution 66: 898-905
Perseke, M., Golombek, A., Schlegel, M. & Struck, T. H.
