Laubierinid snails are associates of crinoids and a modern analogue of Paleozoic platyceratids

Crinoids flourished in the Ordovician, and with that appeared platyceratid gastropods intimately associated with them (Bowsher 1955). This relationship was long-lasting and continued at least to the Permian (Ponder and Lindberg 2008). A classic example of biotic interactions in the fossil record, the prevailing view is that platyceratids were parasites or fed on the excrements of sea lilies (Baumiller and Gahn 2018). Though the phylogenetic affinity of Platyceratidae remains unsettled, anatomical and conchological evidences indicate it is most likely a member of subclass Neritimorpha (Sutton et al. 2006, Nützel et al. 2023). Despite crinoids narrowly surviving the end-Permian extinction, Platyceratidae died out. Since then, no gastropod family has been observed to be specifically linked with crinoids as a whole. The enigmatic gastropod family Laubierinidae is restricted to the deep sea, and because almost all of its sparse records are from dredge hauls and beam trawlings, little information has been available on its ecology (Warén and Bouchet 1990). Here, we demonstrate, based on the first in situ observations covering all four genera, that this family is an obligate associate of crinoids and a modern analogue of platyceratids. Laubierinidae (subclass Caenogastropoda, superfamily Tonnoidea) inhabits the deep sea between approximately 200–4000 m depth (Warén and Bouchet 1990), with four currently recognized genera including Akibumia, Laminilabrum, Laubierina, and Pisanianura containing just one or two extant species each (Strong et al. 2019). Across four separate research cruises to the Atlantic and Pacific oceans (for extended materials and methods see Appendix S1), we encountered all four genera living on crinoids (Figure 1)—strongly reminiscent of fossil platyceratids. These include Akibumia orientalis on a Thalassometra comatulid 2602 m deep in the southern Atlantic (Figure 1A–D), Laminilabrum breviaxe on the stalked Metacrinus rotundus 519 m deep off Kagoshima in Japan (Figure 1E–G), Pisanianura grimaldii on antedonid feather stars 1445 m deep in the northwestern Pacific (Figure 1H,I), and Laubierina individuals on a hyocrinid 1883 m deep also in the northwestern Pacific (Figure 1K–N). Although the Laubierina specimens lacked teleoconch whorls and could not be identified to species level morphologically, molecular barcoding allowed their identification as Laubierina peregrinator (see Appendix S1). In our numerous encounters with laubierinids at the seafloor, all were associated with crinoids. Together with a previous record of Laminilabrum breviaxe on a crinoid stem dismissed as fortuitous (Warén and Bouchet 1990), these strongly support laubierinids as obligate associates of crinoids. This is only the third living gastropod family potentially specialised as parasites of echinoderms, after Eulimidae and Chauvetiidae (Takano and Kano 2014). We found feeding marks (Figure 1K,L) by Laubierina peregrinator that appeared to be drillholes (also previously observed in platyceratids; Baumiller and Gahn 2018) concurrent with damage and discoloration of the surrounding host tissue; however, dissections did not reveal evidence of crinoid remains in the digestive tract. It is therefore likely that laubierinids feed on the body fluid of crinoids. Detailed imagery (for methods see Appendix S1) of the feeding marks using X-ray micro-computed tomography (μ-CT) and scanning electron microscopy (SEM) revealed the removal of the host surface tissue with different morphological details for holes made on the dorsal and ventral surfaces of the crinoid arm (Figure 2). Although we are unaware of feeding marks from fossil crinoids immediately attributable to laubierinids, there are numerous crinoid fossils with small bite marks and pits made by unidentified animals after the extinction of platyceratids (Gorzelak and Salamon 2009). It is possible that some of these are linked to laubierinids or their ancestors, and we hope our imagery will help identify such cases from fossil feeding traces in order to further explore the history of this association in the geological record. A series of publicly available imagery of two Laubierina snails (as unidentified “snails”) by the NOAA (National Oceanic and Atmospheric Administration) research ship Okeanos Explorer in the northern Pacific at 2242 m deep (NOAA Office of Ocean Exploration and Research 2017; see citation for a link) offers further insights, with the larger Laubierina extending its proboscis onto the crinoid's calyx for a prolonged period but without rasping action of the radula. An adult P. grimaldii was also seen positioning its proboscis on the calyx of a comatulid (Figure 1I). We interpret this action as likely coprophagous, parasitic, or both, which has also been hypothesized for platyceratids (Sutton et al. 2006, Baumiller and Gahn 2018). Laubierinids may adopt two or more feeding modes to sustain themselves energetically or exhibit ontogenetic shifts in feeding ecology, as has been suggested for platyceratids (Baumiller 2002). The positions of laubierinids on crinoids elevated well off the seafloor might provide an advantage for filter-feeding as well. In Laubierina, neotenic and sexually mature males still in their protoconchs have been found, while large specimens with teleoconchs were females—leading to the hypothesis that this family exhibits protandrous hermaphroditism (Warén and Bouchet 1990). Our small L. peregrinator specimens (Figure 1K–N) were also neotenic males, confirming that they already live a benthic life (Figure 1J). Furthermore, in the Okeanos Explorer observation, a pair of Laubierina was filmed with a small neotenic individual (presumably male) sitting on the shell of a larger (presumably female) individual laying egg capsules on a crinoid stem. Our Akibumia also laid about a dozen egg capsules (about 3 × 5 mm each) on the crinoid's cirri (Figure 1C), and we also observed egg capsules of P. grimaldii (Figure 1I). In all cases, the capsules were similar to those of other tonnoideans (Gofas and Beu 2002). Like many other tonnoideans, laubierinids are inferred from their multispiral protoconchs to have extremely long larval dispersal periods, which may lead to global distributions. For example, Akibumia orientalis was previously recorded from South Africa to New Zealand to the Azores (Gofas and Beu 2002), and we substantiate the conspecificity of our Atlantic specimen with an Australian specimen (Strong et al. 2019) supported by a pairwise distance of just 2.4% in the cytochrome c oxidase subunit I (COI) gene. The tonnoidean characteristically multispiral, cancellate protoconch (Figure 1N) also leads us to reject the possibility that laubierinids are closely related to platyceratids with tightly coiled protoconchs lacking similar sculptures (Nützel et al. 2023), underscoring two independent origins of parasitism on crinoids between these two families. The oldest known fossil laubierinid is from the Oligocene deposits in southern France (Pisanianura aturensis) (Warén and Bouchet 1990), congruent with an Eocene origin around 34.6 million years ago signposted by a fossil-calibrated multigene phylogenetic analysis (Strong et al. 2019). As such, after the extinction of platyceratids in the end-Permian no gastropod family specialised entirely on crinoids for over 200 million years—although this could also be an artifact from an incomplete fossil record or that feeding marks belonging to related gastropods have not been identified as such, and notably some members of Eulimidae do parasitize crinoids (Takano and Kano 2014). A notable finding among our observations is that laubierinids interact with both stalked crinoids and comatulids. Since feather stars did not evolve until the Jurassic, all crinoids were stalked during the days of platyceratids (Hess 2014). Given that laubierinid snails radiated since the Eocene, they had access to both stalked and unstalked hosts and therefore likely evolved to parasitize both. Like eulimids, laubierinids appear to exhibit differing degrees of association with their hosts, such as the persistent attachment on stalked crinoids in Laminilabrum and more loosely associated ones like Pisanianura living next to comatulids (Figure 1I). Whether each genus is linked with a specific crinoid type remains to be seen. The enlarged osphradium in laubierinids may be used to detect specific types of crinoids for settlement (Warén and Bouchet 1990). Our discovery of the laubierinid-crinoid association provides a direct modern analogue to interpreting the life of platyceratids and highlights the importance of in situ observations in understanding the ecology and behavior of rare deepwater taxa. However, details about their ecology and interactions warrant further studies. Perhaps still in many ways, we know more about platyceratids than laubierinids, but we have the fortunate opportunity to change this in the future as the latter is very much alive today. Chong Chen conceived and designed the project. Ruiyan Zhang, Dongsheng Zhang, Jian-Wen Qiu, and Yadong Zhou collected and sorted specimens at sea. All authors contributed photographs that made up the figures. Chong Chen drafted the manuscript, which was critically revised by Ruiyan Zhang, Jian-Wen Qiu, and Yadong Zhou. We thank the captain and crew on-board R/Vs Shen Hai Yi Hao (cruises DY80, DY83-I, and DY86) and Natsushima (cruise NT11-21; PI: Hiroki Matsuda) for their great support and extend the same gratitude to the HOV Jiaolong and ROV Hyper-Dolphin teams. Marc P. Eléaume (Muséum National d'Histoire Naturelle) is gratefully acknowledged for identifying the comatulid in the genus Thalassometra. We are indebted to NOAA for making imagery from their encounter with Laubierina openly available online, which was extremely valuable—as were online databases of JAMSTEC including DARWIN and J-EDI. This study was supported by the National Key Research and Development Program of China (grant number 2023YFC2812903), the United Nations Ocean Decade Programme Digital DEPTH, and the International Seabed Authority's Sustainable Seabed Knowledge Initiative: One Thousand Reasons Campaign (co-financed by the European Maritime and Fisheries Fund of the European Union, Project 101071214—SSKI-I—EMFAF-2021-ISA-SSKI-IBA). Miwako Tsuda (JAMSTEC) is thanked for helping to obtain the COI sequences, and Katsunori Kimoto (JAMSTEC) for his help in μ-CT scanning. Constructive comments from José H. Leal (Bailey-Matthews National Shell Museum & Aquarium) and an anonymous reviewer improved an earlier version. The authors declare no conflicts of interest. Genetic sequences are available in the National Center for Biotechnology Information GenBank database under accession numbers PQ451241, PQ451242, PQ774871, and PQ774872, at https://www.ncbi.nlm.nih.gov/nuccore/PQ451241, https://www.ncbi.nlm.nih.gov/nuccore/PQ451242, https://www.ncbi.nlm.nih.gov/nuccore/PQ774871, and https://www.ncbi.nlm.nih.gov/nuccore/PQ774872, respectively. The original μ-CT image stack (Chen et al. 2025) is available on Figshare at https://doi.org/10.6084/m9.figshare.27633924.v3. The 3D model of the crinoid arm with Laubierina feeding marks is publicly available on Sketchfab (https://skfb.ly/ptVrQ). The NOAA images and video quoted in the text are from the April-May 2017 “Mountains in the Deep” expedition (EX1705), the data from which are openly available from the following link: https://www.ncei.noaa.gov/waf/okeanos-rov-cruises/ex1705/. Appendix S1. 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