More is needed—Thousands of loci are required to elucidate the relationships of the ‘flowers of the sea’ (Sabellida, Annelida)
Graphical abstract
Introduction
Sabellida is a diverse group of tube-dwelling annelids with radiolar crowns. These generally sessile worms use their crown for respiration and to gather suspended food particles from the water column, as the remaining body stays within the tube. The often colorful appearance of these crowns and their rapid withdrawal into the safety of the tubes, have for long attracted scientists and SCUBA divers alike, resulting in their common names fan worms, feather-duster worms and the affectionate general epithet “flowers of the sea” (Jones, 1973) (Fig. 1).
Three family-ranked taxa are grouped within Sabellida: Serpulidae Rafinesque, 1815; Sabellidae Latreille, 1825 and Fabriciidae Rioja, 1923 (see Kupriyanova and Rouse, 2008). Traditionally the clade Sabellida included additional taxa. Sabellida sensu Fauchald, 1977, Knight-Jones, 1981 also contained Sabellariidae, which was based on their shared chaetal inversion. However, Kieselbach and Hausen (2008) showed significant differences in the specific chaetal arrangement of Sabellidae and Sabellariidae, suggesting an independent evolution of this pattern. Phylogenomic data suggests that Sabellariidae forms a clade with Spionidae (Andrade et al., 2015, Helm et al., 2018, Weigert and Bleidorn, 2016). Rouse and Fauchald (1997) also placed Siboglinidae (formerly outside Annelida, as Pogonophora and Vestimentifera) and Oweniidae inside Sabellida. These taxa no longer form a clade with Sabellidae, Fabriciidae and Serpulidae according to molecular data (Andrade et al., 2015, Helm et al., 2018, Weigert and Bleidorn, 2016). Following this evidence, in this study we restrict the name Sabellida to the clade composed of Fabriciidae, Sabellidae and Serpulidae.
The close affinity of serpulids, the calcareous-tube worms, and sabellids (previously including fabriciids) has long been accepted and supported by a variety of morphological features such as the unique kind of chaetal inversion (Kieselbach and Hausen, 2008), an inverted faecal groove, and a radiolar crown (Dales, 1962, Fauchald, 1977, Fitzhugh, 1989). The phylogenetic relationships within Sabellida have been less clear from morphological data matrices and PCR-based sequence data (Brown et al., 1999, Capa et al., 2011a, Colgan et al., 2006, Dales, 1962, Fauchald, 1977, Fitzhugh, 1989, Kupriyanova and Rouse, 2008, Rouse and Fauchald, 1997, Rousset et al., 2007, Rousset et al., 2004, Smith, 1991, Struck et al., 2007, Zrzavý et al., 2009). Though the monophyly of Serpulidae is well supported (Kupriyanova et al., 2006), the former delineation of Sabellidae (including fabriciids) was shown to be paraphyletic based on sequences from three nuclear genes (Kupriyanova and Rouse, 2008). Therefore, Fabriciinae were removed from Sabellidae, and elevated to Fabriciidae and Sabellidae membership was reduced to the previous subfamily Sabellinae (Kupriyanova and Rouse, 2008). Further, the relationships within Sabellidae have not been resolved with confidence (Capa et al., 2011a). Sabellida has been the focus of interest with regards to life history evolution since they show a wide range of reproductive modes and body sizes (Rouse and Fitzhugh, 1994, Kupriyanova et al., 2001, Rouse et al., 2006). However, without a reliable phylogeny for the group, robust inferences about transformations in life history characters cannot be made.
Transcriptomic datasets of hundreds or thousands of genetic loci have recently transformed the understanding of the annelid tree of life (Andrade et al., 2015, Helm et al., 2018, Struck et al., 2015, Weigert et al., 2014, Weigert and Bleidorn, 2016) and have suggested that some relationships cannot be confidently resolved with a small number of loci (Stiller et al., 2020). A phylogenomic analysis is still missing for the three lineages of Sabellida and within Sabellidae.
The main aim of this study is to resolve the phylogeny of Sabellida, first to elucidate the relationships of the three main lineages and with specific focus on the diversity of Sabellidae. Nineteen new sabellid transcriptomes were sequenced for this study resulting in a sequence matrix containing up to 3015 orthologous genes and around one million amino acid positions. We find a topology among the Sabellida lineages that differs from previous analyses based on few genes. We therefore conducted a thorough methodological analysis using up to 13,393 gene trees to test what effect adding more and more gene trees had on the robustness of the new sabellid phylogeny.
Section snippets
Taxon sampling and transcriptome sequencing
Nineteen species of Sabellida were sampled for de novo transcriptome sequencing in addition to a published transcriptome. The available transcriptome of Prionospio sp. (Spionidae) was selected as an outgroup based on recent phylogenomic studies that supported Spionidae as sister to Sabellida (Andrade et al., 2015, Struck et al., 2015). Specimen details, voucher information and accession numbers for the sequence data are summarized in Table 1. Amphiglena has cryptic diversity in the
Data analyses and matrix assembly
Assembly statistics and values to assess the quality of each transcriptome, together with the number of orthologous genes identified are summarized in Table S1. The smallest number of reads in the total data set was 26.8 million reads for Sabellastarte magnifica (Shaw, 1800) (assembled into 19,577 contigs), whereas the largest one was the outgroup Prionospio sp., with 68.6 million reads (assembled into 37,158 contigs).
Total number of orthologous genes identified across the terminals was 13,393
Discussion
Our phylogenomic study using a large dataset with 21 transcriptomes resolved the main relationships within Sabellida with strong support (Fig. 2, Fig. 3). Our results confidently placed Fabriciidae as sister to a clade of Serpulidae + Sabellidae. This result differs from previously published studies that found Fabriciidae to be the sister group to Serpulidae, though based on few genes (Kupriyanova and Rouse, 2008, Capa et al., 2011a). Our analyses suggest that this discrepancy is due to there
CRediT authorship contribution statement
Ekin Tilic: Conceptualization, Investigation, Formal analysis, Visualization, Writing - original draft. Erfan Sayyari: Methodology, Formal analysis, Visualization, Writing - review & editing. Josefin Stiller: Investigation, Formal analysis, Writing - review & editing. Siavash Mirarab: Conceptualization, Methodology, Writing - review & editing, Supervision. Greg W. Rouse: Conceptualization, Investigation, Writing - review & editing, Supervision.
Acknowledgements
ET was supported by a personal postdoc fellowship of the German Research Foundation, DFG (TI 973/1-1). We gratefully acknowledge Dewy White for her support for this project. We also thank Avery Hatch and Jose Ignacio Carvajal for their help with the molecular lab work and to Charlotte Seid for handling and cataloging of specimens at the Benthic Invertebrate Collection of Scripps Institution of Oceanography. Thanks to Stephen Atkinson and Maria Cristina Gambi for providing samples of Manayunkia
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