Spaghetti to a Tree: A Robust Phylogeny for Terebelliformia (Annelida) Based on Transcriptomes, Molecular and Morphological Data

Abstract

Terebelliformia-"spaghetti worms" and their allies-are speciose and ubiquitous marine annelids but our understanding of how their morphological and ecological diversity evolved is hampered by an uncertain delineation of lineages and their phylogenetic relationships. Here, we analyzed transcriptomes of 20 terebelliforms and an outgroup to build a robust phylogeny of the main lineages grounded on 12,674 orthologous genes. We then supplemented this backbone phylogeny with a denser sampling of 121 species using five genes and 90 morphological characters to elucidate fine-scale relationships. The monophyly of six major taxa was supported: Pectinariidae, Ampharetinae, Alvinellidae, Trichobranchidae, Terebellidae and Melinninae. The latter, traditionally a subfamily of Ampharetidae, was unexpectedly the sister to Terebellidae, and hence becomes Melinnidae, and Ampharetinae becomes Ampharetidae. We found no support for the recently proposed separation of Telothelepodidae, Polycirridae and Thelepodidae from Terebellidae. Telothelepodidae was nested within Thelepodinae and is accordingly made its junior synonym. Terebellidae contained the subfamily-ranked taxa Terebellinae and Thelepodinae. The placement of the simplified Polycirridae within Terebellinae differed from previous hypotheses, warranting the division of Terebellinae into Lanicini, Procleini, Terebellini and Polycirrini. Ampharetidae (excluding Melinnidae) were well-supported as the sister group to Alvinellidae and we recognize three clades: Ampharetinae, Amaginae and Amphicteinae. Our analysis found several paraphyletic genera and undescribed species. Morphological transformations on the phylogeny supported the hypothesis of an ancestor that possessed both branchiae and chaetae, which is at odds with proposals of a "naked" ancestor. Our study demonstrates how a robust backbone phylogeny can be combined with dense taxon coverage and morphological traits to give insights into the evolutionary history and transformation of traits.

May the Palps Be With You – New Insights Into the Evolutionary Origin of Anterior Appendages in Terebelliformia (Annelida)

“…According to the current knowledge (Orrhage 2001) and our presented data, a similar neuroanatomy can be assumed for Pectinariidae as being the sister taxon of all other Terebelliformia (Stiller et al 2020). Many authors also support the homology of the buccal tentacles in all Terebelliformia investigated so far (Holthe 1986;Orrhage 2001;Zhadan and Tzetlin 2002).…”

“…The ampharetid Hypania invalida bears four pairs of digitate branchiae grouped dorsally on the head, while the two terebellid species Lanice conchilega and Terebella lapidaria show three pairs of dichotomous branchiae serially arranged along the trunk (Capa and Hutchings 2006;Stiller et al 2020). The putative basally-branching Pectinariidae also exhibit four pairs of branchiae along the segments II-V like shown for many other Terebelliformia (Nogueira et al 2010(Nogueira et al , 2013.…”

“…However, phylogenomic approaches placed Terebelliformia con dently within the Sedentaria and hence they represent the sister taxon to the Maldanomorpha (Maldanidae + Arenicolidae) (Weigert et al 2014a;Helm et al 2018). Recently, new analyses uncovered the phylogenetic relations within the group, and suggest a taxon of Ampharetidae + Alvinellidae and Trichobranchidae + Terebellidae (including Melinnidae) (Stiller et al 2020). Furthermore, the authors present Pectinariidae as sistergroup to all other Terebelliformia and therefor recover the idea of an "archaeoterebellomorph" with four pairs of branchiae and a large prostomuim (Holthe 1986).…”

“…The position of these buccal tentacles differs inside the Terebelliformia and reaches from tentacles surrounding the mouth opening in an arc-like frame (in Pectinariidae), over appendages originating from an evertable pharynx (in Ampharetidae) to tentacles located in a dorsal position on the anterior end (in Terebellidae and Trichobranchidae) (Zhadan and Tzetlin 2002;Stiller et al 2020). So far, two contradictory theories about the evolutionary origin of these buccal tentacles in Terebelliformia are debated:…”

Annelids of the eastern Australian abyss collected by the 2017 RV ‘Investigator’ voyage

“… Melinnidae are tubicolous annelids that often have dorsal hooks. Recently the subfamily Melinninae Chamberlin, 1919 within Ampharetidae was raised to the family Melinnidae ( Stiller et al 2020 ). The family Melinnidae is composed of five accepted genera and 49 species ( Read and Fauchald 2020 ).…”