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Current Status of Annelid Phylogeny

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Current Status of Annelid Phylogeny Org Divers Evol (2016) 16:345–362 DOI 10.1007/s13127-016-0265-7 REVIEW Current status of annelid phylogeny Anne Weigert1 & Christoph Bleidorn1,2 Received: 27 August 2015 /Accepted: 16 January 2016 /Published online: 30 January 2016 # Gesellschaft für Biologische Systematik 2016 Abstract Annelida is an ecologically and morphologically simplifications of body plan as adaptations to new life styles diverse phylum within the Lophotrochozoa whose members can be found. Therefore, annelids will be an appropriate mod- occupy a wide range of environments and show diverse life el to understand major transitions in the evolution of Bilateria styles. The phylogeny of this group comprising more than 17, in general. Evolutionary developmental studies are one way to 000 species remained controversial for a long time. By using investigate macroevolutionary transition in annelids. We next-generation sequencing and phylogenomic analyses of briefly summarize the state of developmental model organ- huge data matrices, it was finally possible to reach a well- isms in Annelida and also propose new candidates on the supported and resolved annelid backbone tree. Most annelid background of the phylogeny. diversity is comprised in two reciprocal monophyletic groups, Sedentaria and Errantia, which are named after the predomi- Keywords Annelida . Evo-devo . Evolution . Model nant life style of their members. Errantia include Aciculata organism . Phylogenomics . Polychaeta (Phyllodocida + Eunicida) and Protodriliformia, which is a taxon of interstitial polychaetes. Sedentaria comprise most of thepolychaetefamiliesformerlyclassifiedasCanalipalpataor Annelid phylogeny—a historical perspective Scolecida, as well as the Clitellata. Six taxa branch as a basal grade outside of this major radiation: Oweniidae, Annelida, commonly referred to as segmented or ringed Magelonidae, Chaetopteridae, Sipuncula, Amphinomida, worms, is an ecologically diverse phylum within the and Lobatocerebrum. Oweniidae and Magelonidae form a Lophotrochozoa whose members occupy a wide range of en- monophyletic group which we name Palaeoannelida, which vironments including terrestrial, limnic, and marine habitats constitutes the sister taxon of the remaining annelids. The (Rouse and Pleijel 2001;Aguadoetal.2014). Several species early splits of annelid phylogeny date back to the Cambrian. are highly specialized to distinct ecological niches such as The new annelid phylogeny highlights the variability and la- intertidal and pelagic zones or hydrothermal vents. In addi- bility of annelid body plans, and many instances of tion, annelids exhibit a huge diversity of body and larval forms, life modes, and feeding strategies and possess true segmentation, which is otherwise found only in Arthropoda This article is part of the Special Issue. The new animal phylogeny: The and Chordata (Seaver 2003). The combination of these fea- first 20 years tures makes Annelida a subject of intense phylogenetic re- * Anne Weigert search to understand their evolution. Up to date, around 17, [email protected] 000 described species are recognized (Zhang 2011), but their overall systematics were unclear in the past. Formerly, the Annelida were classified into four groups: Archiannelida, 1 Molecular Evolution and Animal Systematics, University of Leipzig, Polychaeta, Oligochaeta, and Hirudinea (Grube 1850; Talstr. 33, 04103 Leipzig, Germany Hatschek 1878;Lamarck1818). Additionally, several inver- 2 German Centre for Integrative Biodiversity Research (iDiv) tebrate taxa like Echiura, Pogonophora, Myzostomida, and Halle-Jena-Leipzig, Deutscher Platz 5e, 04103 Leipzig, Germany Sipuncula were regarded as closely related to Annelida, but 346 A. Weigert, C. Bleidorn mainly considered as own separate phyla, and therefore ex- interstitium (Hermans 1969). Formerly, they were considered cluded from the annelid radiation (Graff 1877; Johansson as a monophyletic group within Annelida, either as part of 1937;Newby1940). The classification of annelids has Polychaeta or forming the basal radiation of annelids, or even changed drastically many times, resulting in competing hy- their own phylum, and included five families: Dinophilidae, potheses based on different character sets. Here, we summa- Nerillidae, Polygordiidae, Protodrilidae, and Saccocirridae rize the main changes and developments in the phylogenetic (Westheide 2008). However, during the twentieth century history of Annelida. this hypothesis of a common ancestor of the interstitial annelids remained controversial. Consequently the Morphology-based classifications BArchiannelida^ were regarded as an artificial grouping with an independent adaptation to the interstitium of sev- Polychaete phylogeny: A problem in protostome evolution eral members leading to a simplified body plan either by was the title of a review article by Kristian Fauchald published miniaturization or progenetic evolution (Fauchald 1977; in 1974, summarizing the history and foreshadowing future Purschke and Jouin 1988). problems of reconstructing the phylogeny of Annelida (Fauchald 1974). We will briefly summarize morphology- Clitellata based classifications concentrating on the two main groups which have been distinguished: polychaetes and clitellates. Characterized by the presence of a cocoon-forming clitellum For more detailed reviews please refer to Struck (2013b and during part of their life cycles, hermaphroditism, and the ab- Fauchald and Rouse (1997). sence of parapodia, the clitellates traditionally comprised the Oligochaeta, possessing a few chaetae, and leeches Polychaeta (Hirudinea), which completely lack chaeta (Brusca and Brusca 2003). According to their simplified appearance they The Polychaeta or bristle worms comprise most of the diver- were regarded as a separate class from other annelids and their sity of annelids. They mostly live in marine habitats and are monophyly was convincingly supported (Grube 1850;Dales characterized by parapodia-bearing chitinous chaetae, and 1963;Fauchald1977; Rouse and Fauchald 1997). were first separated from clitellate annelids by Grube (1850). The most widely used system of polychaete classification dur- Molecular phylogenetics of Annelida ing the twentieth century was the division into two groups, mainly based on the observed lifestyle and feeding strategies By the end of the twentieth century, the first molecular phylo- (Quatrefages 1865;Fauvel1923): Errantia, uniting the more genetic analyses focusing on annelid relationships were pub- or less free moving and predatory forms, and Sedentaria, com- lished. A short overview of the development and achieve- prising the often sessile and tube-dwelling forms. This classi- ments of annelid molecular phylogenetics follows. fication did not intend to depict evolutionary relationships and was replaced by the first thorough morphological cladistic Single gene analyses analysis by Rouse and Fauchald (1997), who subdivided Polychaeta into two separate taxonomic clades: Palpata and The first molecular studies including annelid taxa usually an- Scolecida (Fig. 1). The Palpata were characterized by the pos- alyzed 18S rRNA or elongation factor 1α gene sequences session of palps and were further subdivided into two distinct (Winnepenninckx et al. 1995; Kim et al. 1996; McHugh groups: Canalipalpata, which feature the presence of peristo- 1997;Kojima1998; Winnepenninckx et al. 1998;Eeckhaut mial grooved palps and include mainly burrowing deposit et al. 2000; McHugh 2000; Struck et al. 2002a; Bleidorn et al. feeders or sessile tube dwelling filter feeders (Sabellida, 2003a, b). At first, the availability of data was increasing Spionida, Terebellida), and Aciculata, which are characterized slowly and taxon sampling was low, covering only a fraction by the presence of aciculae (internalized supporting chaetae) of the annelid diversity. Higher ranked polychaete taxa as and include members with a more mobile life style, actively postulated by Rouse and Fauchald (1997)(Aciculata, foraging and predating (Eunicida, Phyllodocida). The Canalipalpata, Scolecida), or even Annelida and Polychaeta Aciculata resembled more or less the Errantia adapted by could not be recovered as monophyletic, since outgroups were Fauvel (1923). The Scolecida completely lack palps and head branching between annelid taxa. Furthermore, the resolution appendages and include mostly burrowing and deposit feed- of relationships among families was poor and highly inconsis- ing taxa, as, e.g., Orbiniidae, Arenicolidae, or Opheliidae. A tent between analyses. Whereas the monophyly of many an- group of difficult to place polychaete worms were the nelid families could be corroborated, the relationships among BArchiannelida^. They comprise a number of interstitial them remained largely obscure (Bleidorn 2009). Currently, worms, which are characterized by the lack of body or head molecular data for the 18S rRNA is available for almost all appendages,whichisregardedasanadaptationtothe major annelid families, but unfortunately this marker alone Current status of annelid phylogeny 347 Fig. 1 Annelid phylogeny according to Rouse and Fauchald (1997) based on morphology. Annelida are split into Polychaeta and Clitellata. Polychaeta com- prise Palpata (Canalipalpata and Aciculata) and Scolecida has proven to be insufficient for resolving annelid relation- instances) their combination with morphological characters ships, especially for deeper nodes. However, the incorporation was an increase of the recovery of several monophyletic an- of molecular data
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