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New Genera and Species from the Equatorial Pacific Provide Phylogenetic Insights Into Deep-Sea Polynoidae (Annelida)

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New Genera and Species from the Equatorial Pacific Provide Phylogenetic Insights Into Deep-Sea Polynoidae (Annelida) Downloaded from https://academic.oup.com/zoolinnean/advance-article-abstract/doi/10.1093/zoolinnean/zly063/5181329 by GEOMAR Bibliothek Helmholtz-Zentrum für Ozeanforschung user on 07 December 2018 Zoological Journal of the Linnean Society, 2018, XX, 1–81. With 22 figures. New genera and species from the Equatorial Pacific provide phylogenetic insights into deep-sea Polynoidae (Annelida) PAULO BONIFÁCIO*, AND LÉNAÏCK MENOT Ifremer, Centre Bretagne, REM EEP, Laboratoire Environnement Profond, ZI de la Pointe du Diable, CS 10070, F-29280 Plouzané, France Received 3 October 2017; revised 11 July 2018; accepted for publication 9 August 2018 Polynoidae contains ~900 species within 18 subfamilies, some of them restricted to the deep sea. Macellicephalinae is the most diverse among these deep-sea subfamilies. In the abyssal Equatorial Pacific Ocean, the biodiversity of benthic communities is at stake in the Clarion-Clipperton Fracture Zone (CCFZ) owing to increased industrial interest in polymetallic nodules. The records of polychaetes in this region are scarce. Data gathered during the JPI Oceans cruise SO239 made a significant contribution to fill this gap, with five different localities sampled be- tween 4000 and 5000 m depth. Benthic samples collected using an epibenthic sledge or a remotely operated ve- hicle resulted in a large collection of polynoids. The aims of this study are as follows: (1) to describe new species of deep-sea polynoids using morphology and molecular data (COI, 16S and 18S); and (2) to evaluate the monophyly of Macellicephalinae. Based on molecular and morphological phylogenetic analyses, ten subfamilies are synonymized with Macellicephalinae in order to create a homogeneous clade determined by the absence of lateral antennae. Within this clade, the Anantennata clade was well supported, being determined by the absence of a median antenna. Furthermore, 17 new species and four new genera are described, highlighting the high diversity hidden in the deep. A taxonomic key for the 37 valid genera of the subfamily Macellicephalinae is provided. ADDITIONAL KEYWORDS: deep sea – identification key – molecular systematics – morphology – new genera – new species – phylogeny – Polychaeta. INTRODUCTION more rarely, analogous habitats, such as submarine caves in shallow waters (i.e. Admetellinae Uschakov, The family Polynoidae Kinberg, 1856 is one of six 1977, Bathyedithinae Pettibone, 1976, Bathymacellinae families called scale worms (Aphroditiformia). With Pettibone, 1976, Branchinotogluminae Pettibone, ~900 species belonging to 167 genera in 18 subfamilies 16August2018 1985a, Branchiplicatinae Pettibone, 1985b, (Wehe, 2006; Norlinder et al., 2012; Read & Fauchald, Branchipolynoinae Pettibone, 1984a, Eulagiscinae 2018), polynoids are the most diverse polychaetes Pettibone, 1997, Lepidonotopodinae Pettibone, in number of genera and the second most diverse in 1983, Macellicephalinae Hartmann-Schröder, 1971, number of species (Hutchings, 2000; Wehe, 2006; Macellicephaloidinae Pettibone, 1976, Macelloidinae Read & Fauchald, 2018). They are errant worms with Pettibone, 1976, Polaruschakovinae Pettibone, 1976 and wide-ranging distribution, from shallow intertidal Vampiropolynoinae Marcus & Hourdez, 2002). Deep-sea waters to hadal trenches (Hartmann-Schröder, 1974; polynoids typically have different numbers of cephalic Fauchald, 1977; Hutchings, 2000). However, 13 sub- appendices compared with their shallow-water counter- families appear to be restricted to the deep sea (mostly parts. The usual form of the polynoid prostomium bears below 500 m depth), from bathyal to hadal depths, three antennae (one median antenna and two lateral including specialized chemosynthetic habitats and, antennae) and is commonly observed in shallow waters but also in few deep-sea subfamilies (i.e. Admetellinae, *Corresponding author. E-mail: [email protected] [Version of Record, published online 14 November 2018; Bathymacellinae and Eulagiscinae). The main features http://zoobank.org/urn:lsid:zoobank.org:pub:74C07292 differentiating the other deep-sea subfamilies are the -2BD6-4E3E-B68DB144B81BBD83] absence of lateral antennae (Branchinotogluminae, © Zoological Journal of the Linnean Society 2018, 2018, XX, 1–81 1 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons. org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Downloaded from https://academic.oup.com/zoolinnean/advance-article-abstract/doi/10.1093/zoolinnean/zly063/5181329 by GEOMAR Bibliothek Helmholtz-Zentrum für Ozeanforschung user on 07 December 2018 2 P. BONIFÁCIO AND L. MENOT Branchiplicatinae, Branchipolynoinae, Branchipolynoinae has four species in one genus Macellicephalinae, Macellicephaloidinae, and Branchiplicatinae one species in one genus. The Macelloidinae, Lepidonotopodinae and high number of monotypic subfamilies and genera Vampiropolynoinae) or the complete absence of anten- observed in deep-sea polynoids raises concerns and nae (Bathyedithinae and Polaruschakovinae). The suggests either that subfamilies do not represent subfamilies Branchinotogluminae, Branchiplicatinae, monophyletic groups and should be reviewed in a Branchipolynoinae, Lepidonotopodinae, phylogenetic context or that there is a high diversity Macellicephalinae (genera Bathykurila Pettibone, of as yet undiscovered species within these subfami- 1976 and Levensteiniella Pettibone, 1985c) and lies/genera, the discovery of which might support the Vampiropolynoinae have been successful in exploiting monophyly of these groupings. Based only on morpho- deep-sea chemosynthetic ecosystems, such as hydro- logical data, the paraphyly of Polynoidae subfamilies thermal vents and cold seeps (Pettibone, 1983, 1984a, has already been suggested by Rouse & Pleijel (2001), 1985a, b, 1986; Marcus & Hourdez, 2002). Many of these who stressed the need to investigate these in a phylo- subfamilies [Branchinotogluminae, Branchiplicatinae, genetic framework. Branchipolynoinae and Lepidonotopodinae (genus The phylogeny and evolutionary origin of the sub- Thermopolynoe Miura, 1994)] exhibit a rare char- family Macellicephalinae within polynoids is still un- acteristic within polynoids, namely the presence of clear. Phylogenetic studies that included Polynoidae to branchiae, which is considered an adaptation to living date were mainly concerned with phylogeny of Annelida in hypoxic environments (Hourdez & Jouin-Toulmond, (Rouse & Fauchald, 1997; Zrzavy et al., 2009) or the 1998; Hourdez & Lallier, 2007). The other abranchi- deeper relationships of scale worms (Aphroditiformia) ate deep-sea subfamilies are more widespread in at the family level (Wiklund et al., 2005; Norlinder hadal trenches, at abyssal depths, in canyons and in et al., 2012; Gonzalez et al., 2018). With regard to submarine caves (Levenstein, 1962; Pettibone, 1976; Macellicephalinae, Uschakov (1977, 1982) suggested Gonzalez et al., 2017). the presence of derived character states in the worms The first species described from the deep-sea en- from this subfamily (e.g. short body and reduction of vironment was Polynoe (Macellicephala) mirabilis jaws), hypothesizing that they originated from a com- McIntosh, 1885, collected from off the coast of New mon ancestor with genus Bathymoorea Pettibone, Zealand during the Challenger Expedition (1280 1967. Two studies using combined morphological and m depth, station 169, 37°34′S, 179°22′E). The sub- molecular data have already suggested the paraphyly family Macellicephalinae was erected by Hartmann- of the subfamily Macellicephalinae. Norlinder et al. Schröder (1971) in order to group the genus (2012) showed a well-supported clade (three represent- Macellicephala McIntosh, 1885 and other representa- atives of deep-sea subfamilies) with members of the tives from great oceanic depths fitting the following subfamilies Macellicephalinae, Branchinotogluminae diagnosis: median antenna absent or present; and lateral antennae absent. In a review of the 37 known and Branchipolynoinae. However, owing to the limited species, which were attributed, directly or indir- number of sequences from deep-sea subfamilies avail- ectly, to the subfamily Macellicephalinae, Pettibone able, no hypothesis about their relationships was (1976) erected five new subfamilies (Bathyedithinae, developed. In a larger, but still limited, number of Bathymacellinae, Macellicephaloidinae, seven representative species of deep-sea subfamilies, Macelloidinae and Polaruschakovinae) and ten new Gonzalez et al. (2017, 2018) recovered two main genera, many of them monotypic. With the produc- clades: (1) Macellicephalinae, Branchinotogluminae tion of taxonomic keys for subfamilies, genera and and Branchipolynoinae, similar to Norlinder et al. species, this remains the most important work con- (2012); and (2) a clade composed only of members cerning the morphological identity of the subfamily of Macellicephalinae. The lack of knowledge about Macellicephalinae and other deep-sea subfamilies of deep-sea polynoids inevitably reflects the small Polynoidae. The subfamily Macellicephalinae is the number of samples, particularly DNA friendly, from most diverse of the deep-sea subfamilies in number the deep sea. The relative larger body size, low density of species and genera, with 36 species in 16 genera, and high mobility of polynoids reduce the probability while Lepidonotopodinae has nine species in two of adequate
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