Deep-sea hydrothermal vents are extreme habitats rich in energy and reduced matters, which support flourished chemosynthesis-based ecosystems and form biodiversity hotspots along the global spreading ridge systems (Van Dover, 2000). One of the most notable features of these vent communities is that they mainly comprise vent endemic fauna, which are not in any other habitats (Wolff, 2005). One of such typical examples is the vent endemic Alvinellidae (Annelida) Desbruyères and Laubier (1982), whose members are notable for their proximity to the fluid sources in hydrothermal vents and excellent adaptations to an extremely high temperature gradient (Jollivet and Hourdez, 2020).

A total of 12 alvinellid species have so far been described and assigned to two genera, Alvinella and Paralvinella. All of them are only known from Pacific hydrothermal vent fields, with the two Alvinella species (Alvinella pompejana Desbruyères and Laubier, 1980 and Alvinella caudata Desbruyères and Laubier, 1986) and three Paralvinella species (Paralvinella grasslei Desbruyères and Laubier, 1982, Paralvinella bactericola Desbruyères and Laubier, 1991 and Paralvinella pandorae irlandei Desbruyères and Laubier, 1986) reported from the East Pacific Rise (EPR) and Guaymas vent fields, four from the northeast Pacific (Paralvinella palmiformis Desbruyères and Laubier, 1986, Paralvinella pandorae pandorae Desbruyères and Laubier, 1986, Paralvinella dela Detinova, 1988 and Paralvinella sulfincola Desbruyères and Laubier, 1993), two from the southwest Pacific vent ecosystems (Paralvinella fijiensis Desbruyères and Laubier, 1993 and Paralvinella unidentata Desbruyères and Laubier, 1993), and one from the Marianas back-arc spreading center and the Okinawa Trough (Paralvinella hessleri Desbruyères and Laubier, 1989). These worms usually form dense aggregations on varied hard substrata, including chimney walls, basaltic cracks with venting fluids and siboglinid tubes (Tunnicliffe et al., 1993; Desbruyères et al., 1994; Hurtado et al., 2004). Although hydrothermal vent organisms usually show a high degree of regional endemism (Rogers et al., 2012), a family endemic to the Pacific vents is still rare. However, the view on this alvinellid biogeographic pattern is challenged by recent discovery of alvinellids in Indian Ocean vents.

Early investigations at Kairei and Edmond vent fields on the Central Indian Ridge (CIR) reported “notable absence” of alvinellids as one of the features that distinguish them from their Pacific counterparts (Van Dover et al., 2001). Investigations in vent fields on the Southwest Indian Ridge (SWIR) (e.g., Longqi and Tiancheng vent fields) and Southeast Indian Ridge (SEIR) (Plegia vent field) also found no signs of such worms (Copley et al., 2016; Zhou et al., 2018; Gerdes et al., 2019). However, at the Solitaire field over 800 km north of Kairei hydrothermal field, a deep-seabed image captured by the Human-Occupied Vehicle (HOV) Shinkai 6500 surprisingly revealed a small patch of alvinellid worms (taxonomically unresolved at general level) associated with the scaly foot snail, Chrysomallon squamiferum Chen et al. (2015), representing the first report of such worms outside the Pacific (Nakamura et al., 2012). In 2017, we collected alvinellid specimens from two vent sites, Daxi and Wocan on the Carlsberg Ridge (CR) in the northwest Indian Ocean. These alvinellids were abundant in the Wocan field, but were not commonly seen in the Daxi field (Wang et al., 2021). Due to the very late discovery of the first active deep-sea hydrothermal vent on the Carlsberg Ridge (almost 15 years after locating the first vent in the Indian Ocean) (Wang et al., 2017), little is known about the diversity of macrobenthos inhabiting the northern Indian Ocean vents, with only a rough description of Daxi vent community at around 6°48′N (Wang et al., 2021). Most of the taxa are undescribed, except for three new species of polychaetes (Zhou et al., 2019; Wang et al., 2020). Since the alvinellid-dominated polychaete assemblage might be unique to the northwest Indian Ocean vents, identifying these alvinellid species and determining their phylogenetic relationships with their Pacific Ocean relatives will enhance our understanding of the divergence history and diversity of this family of vent endemic polychaetes.

An early study using allozyme recovered Alvinella and Paralvinella as two monophyletic groups (Jollivet et al., 1995). Based on DNA data, recent molecular phylogenetic studies recovered Alvinellidae as a monophyletic clade, while Paralvinella is a paraphyletic genus with the sequenced species split into two lineages (Vrijenhoek, 2013; Stiller et al., 2020). One Paralvinella lineage is composed of a pair of sibling geographic species, P. pandorae irlandei in the northeast Pacific and P. pandorae pandorae on the EPR; The other, comprising P. fijiensis (southwest Pacific), P. sulfincola (northeast Pacific), P. grasslei (EPR) and P. palmiformis (northeast Pacific), forms a clade with the Alvinella lineage, and this clade is sister to the P. pandorae lineage (Stiller et al., 2020). To address the issue of paraphyletic status of Paralvinella, Stiller et al. (2020) referred the P. pandorae lineage to Nautalvinella Desbruyères and Laubier, 1993 based on a combined multigene and morphological dataset, which was originally a subgenus in Paralvinella (Desbruyères and Laubier, 1993). Although there are three pairs of sibling geographic species (P. palmiformis/P. grasslei, P. pandorae pandorae/P. pandorae irlandei, and P. dela/bactericola), no sequences from the remaining four Paralvinella species to fully resolve the within-familial phylogeny and biogeographic pattern in the Pacific (Jollivet and Hourdez, 2020). The discovery of alvinellids in the Indian Ocean has raised questions on alvinellid phylogeny and biogeography beyond the Pacific: (1) are the Indian Ocean alvinellids new to science?, (2) do they represent a distinct lineage or not?, and (3) how may this Indian lineage contribute to a better understanding of the biogeography of alvinellids. Aiming to answer these questions, we characterize these alvinellids with a combined morphological and genetic approach.

In the present study, we described a new species of Alvinellidae from northern Indian Ocean hydrothermal vent field and confirmed its placement in the genus Paralvinella using both morphological and genetic evidences. The concatenated phylogeny revealed a branch pattern of three clades (clades I, II, and III in Figure 5) similar to other gene trees, but with higher supports. This three-clades pattern is also largely the same with that recovered in Stiller et al. (2020) except for the positions of P. sulfincola and P. fijiensis in relation to other species in clade III. The subdivision of Paralvinella into three subgenera was proposed by Desbruyères and Laubier (1993) based on traits of branchiae filaments, buccal apparatus, and distributions of the notopodial lobes and the uncinigerous tori (Jollivet and Hourdez, 2020). The subgenus Nautalvinella matches well with Clade I and was referred to Nautalvinella Desbruyères and Laubier (1993) (Stiller et al., 2020), but Paralvinella (Nautalvinella) unidentata is not clustered with this clade in an ultrametric phylogenomic tree recently reconstructed by Jollivet and Hourdez (2020). Similarly, monophyletic cluster of the four Paralvinella (Paralvinella) species (as revealed in Stiller et al., 2020 and Jollivet and Hourdez, 2020) in clade III is likely to be unstable with the addition of the Indian and West Pacific species in the present study. It is currently not possible to determine if the Indian/West Pacific subclade (formed by P. hessleri, Paralvinella sp. ZMBN and P. mira) corresponds to the subgenus Miralvinella due to the lack of morphological data from Paralvinella sp. ZMBN, on one hand, and DNA data from P. bactericola and P. dela, on the other hand. Thus, a wider sampling effort on either taxa or DNA markers is needed to validate the delineation of these species at subgenus level.

The Indian Ocean alvinellids appear to be genetically closer to the West Pacific rather than to the East Pacific counterparts based on either genetic distance calculation or phylogeny inference. Genetic affiliations between Indian and West Pacific counterparts have been shown in a variety of taxa for the vent fauna, such as Bathymodiolus mussels (Breusing et al., 2015), Alviniconcha snails (Johnson et al., 2015), Amphisamytha (Zhou et al., 2019), Archinome jasoni (Borda et al., 2013), resulting in a hypothesis of historical connection between the two regions (Watanabe and Beedessee, 2015). By contrast, two other Wocan polychaetes, Amphisamytha wocanensis (Ampharetidae) and Hesiolyra heteropoda (Hesionidae), temporally exhibit closer genetic relationships with their East Pacific congeners (Zhou et al., 2019; Wang et al., 2020). Although the phylogenetic inference may be modified with the addition of either more DNA markers or more sampling taxa in future, the current results indicate invasion of Paralvinella into northern Indian Ocean from the West Pacific. According to the current phylogeny, the emergence of the West Pacific alvinellid lineages appears to be more recently than their East Pacific relatives, and the latter also exhibit highest phylogenetic diversity (Jollivet and Hourdez, 2020; Stiller et al., 2020). This pattern is closer to the scenario proposed by Bachraty et al. (2009), in which EPR played a central role in the dissemination of vent fauna, although Moalic et al. (2012) tended to put the West Pacific in the central position connecting the other vent fauna provinces. In addition, due to the lack of information on the alvinellid worms collected at the Solitaire vent field on the CIR, we still do not know whether the colonization of the Indian ridge by the Western Pacific alvinellids occurred once or via two independent events.

Whatever the route taken by the ancestors of P. mira to invade the Indian Ocean, this invasion event has undoubtedly changed our view of vent polychaete biogeography in the Indian Ocean. The discovery of P. mira adds to the unique polychaete diversity at northern Indian Ocean hydrothermal vents. Together with the observation of alvinellid worms at the Solitaire vent field, this worm family appears to be absent from all well-characterized hydrothermal vents south of Solitaire, including Edmond, Kairei, Tiancheng, and Longqi (Watanabe and Beedessee, 2015; Copley et al., 2016; Zhou et al., 2018; Gerdes et al., 2019). Notably, distinct dominant polychaete assemblages are recovered at vents across the Indian Ocean Ridges: dorvillids/ampharetids/hesionids at Longqi (on the SWIR, Zhang et al., 2017; Zhou et al., 2018; Wang et al., 2020), amphinomids at Kairei (on the CIR, Watanabe and Beedessee, 2015), and alvinellids/hesionids at Wocan (on the CR, Wang et al., 2020; this study). These differences together with the observed variations of faunal composition on crustaceans and mollusks (the other two dominant taxa in deep-sea hydrothermal vents), result in a high faunal dissimilarity between the SWIR and CIR vent communities and indicate two potential sub-bioregions (Zhou et al., 2018; Sun et al., 2020). As one of the three dominant taxa, the specific polychaete assemblage at the Wocan field reinforces such dissimilarities between CR and CIR/SWIR vent communities and strengthens the point of view that the northern Indian hydrothermal vents may hold a unique biodiversity. This provides new insights toward biogeographic subdivision in the Indian Ocean.

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found in the article.

YZ and CW designed the project. YZ collected and preserved the samples. YH and YZ performed the morphological examination and molecular analyses. All authors drafted the manuscript and contributed to the final version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The handling editor declared a past co-authorship with several of the authors DZ, CW, and YZ.