Syllipsimopodi bideni, Whalen & Landman, 2022

Whalen, Christopher D. & Landman, Neil H., 2022, Fossil coleoid cephalopod from the Mississippian Bear Gulch Lagerstätte sheds light on early vampyropod evolution, Nature Communications 13 (1), pp. 364001-364001 : 3-7

Syllipsimopodi bideni gen. et sp. nov.

Etymology. The genus name is derived from the Greek συλλήψιμος (syllípsimos) for prehensile and πόδι (pódi) for foot. The name prehensile-foot is chosen because this is the oldest known cephalopod to develop suckers, allowing the arms, which are modifications of the molluscan foot, to better grasp prey and other objects. The species name is to celebrate the recently inaugurated (at the time of submission) 46th President of the United States, Joseph R. Biden.

Holotype. ROMIP 64897 (Royal Ontario Museum). Material. The type and only specimen was donated to the Royal Ontario Museum by B. Hawes in 1988; accession number 88-72717. There is no counterpart.

Locality. Bear Gulch Limestone , Heath Formation, Big Snowy Group, Fergus County, Montana, USA 18. The Bear Gulch Limestone is a plattenkalk, or lithographic limestone, similar to the more famous Jurassic Solnhofen Limestone of Germany 19. Deposition occurred in a low-latitude shallow marine bay subject to oscillating semi-arid and tropical conditions18. Exceptional preservation is likely a result of microturbidites deposited by seasonal monsoons18. Monsoonal rainfall would have rapidly introduced terrestrial sediments and biomatter into the bay, feeding algal blooms that created short-lived anoxic zones simultaneous with the saline instability caused by the rapid injection of voluminous freshwater18. Bear Gulch is perhaps best known for the pelagic fauna of the central basin and bay mouth – a diverse array of vertebrates20–22 (especially chondrichthyans22–25 and coelacanthiforms22,26), malacostracans19,27, polychaetes22, and cephalopods13,28–30, which are preserved in such exquisite detail that vascularization can sometimes be distinguished31. Benthic fossils are very rare in the central basin18,22, but marginal facies preserve gastropods, worms, asterozoans, and abundant sponges, which acted as a substrate for various brachiopods, bivalves, and conulariids18,19,22. Crinoids, blastoids, bryozoans, and corals are almost absent; algae (especially dasyclads) are common throughout18,22.

Horizon. Bear Gulch Limestone, Arnsbergian E2b (~328.3–324.5 Ma), Serpukhovian (Namurian), Mississippian, Carboniferous 8,18,32.

Diagnosis. ( Figs. 3 , 4 ) Coleoid with simple, nearly triangular gladius, bearing funnel-like conus and median field with median rib, but no hyperbolar zones, cone flags, or lateral reinforcements; lateral fields unlikely. Lacking chambered phragmocone, primordial rostrum, or rostrum. Ten arms bearing biserial rows of suckers but no hooks or cirri; two arms may be elongated (though this could be taphonomic). Ink sac present. Terminal median fin support and one fin pair present.

Description. The gladius median field is simple; it is widest at the extreme anterior with straight lateral edges and a flat (not rounded/pointed) anterior edge ( Figs. 3a , 4 ). The median asymptote angle is ~13.8°. The gladius length to width ratio is 3.17; the median field is ~6.5 cm long, which is ~55% of the total body length. The median field bears a prominent median rib, which is diagenetically distorted and broken in various places (Supplementary Fig. 2 ). The rib appears to be posteriorly bipartite and anteriorly unipartite ( Figs. 2 , 3 ). Gladius growth lines are poorly preserved and only clearly visible in one place on the lateral edge (Supplementary Fig. 3 ). The funnel-like conus is ~6.8 mm long ( Figs. 2 , 3 ).

A cigar-shaped central fin support measuring ~13.1 mm long is preserved posterior to the gladius ( Fig. 3 ; Supplementary Fig. 4 ); an originally cartilaginous composition seems most likely. It is possible that this fin support is a vestige of the phragmocone, but we consider this alternative unlikely because there is no evidence of a siphuncle or septa. These are unlikely to have been dissolved without leaving a trace since septa can clearly be observed in the co-occurring coleoid Gordoniconus 13. Septa are dissolved in Bear Gulch ammonoids30; but since Gordoniconus is a coleoid, we consider it a better taphonomic comparator. Also, the fin support is posterior to and thus external of the conus; the phragmocone should be internal to the conus ( Fig. 5 ). We consider a primordial rostrum identity unlikely because it seems doubtful that a primordial rostrum (or rostrum) would be present in the absence of a phragmocone. The fin support is associated with patches of a shiny fibrous mineral ( Fig. 3 ; Supplementary Fig. 4 ), presumed to be connective tissue remnants. The holotype appears to preserve a faint outline of a single pair of short terminal lobate fins measuring ~2.3 cm long anteroposteriorly and ~1.7 cm laterally across at the widest position ( Figs. 3 , 4 ).

Ten sucker-bearing arms are preserved, measuring ~2.1–2.4 mm wide at the midlength ( Fig. 4b, c ). Developmental evidence and phylogenetic inference have long suggested that the ten-arm condition is ancestral for cephalopods and vampyropods33–35, but no ten-armed fossils have been documented outside of the decabrachian-belemnoid clade prior to the discovery of Syllipsimopodi . Syllipsimopodi is the first and only known vampyropod to possess ten robust, functional appendages; all other known vampyropods have either reduced arm pair II to filaments (i.e., Prototeuthidina7, Loligosepiina7,36, Teudopseina 7, Vampyromorphida ), or lost the arm pair entirely (i.e., Octopoda ).

Two arms, measuring ~4.0 and ~4.1 cm long (~27% of the total body length), might have been elongated relative to the other eight arms ( Fig. 4b, c ). These elongated arms do not have any obvious manus, as in decabrachian tentacles, and are not significantly thinner than the unmodified arms, as in vampyromorph filaments ( Fig. 4b, c ). Of the shorter arms, the three best preserved measure ~1.7, ~1.9, and ~1.9 cm long, respectively (~13% of the total body length); the remaining five arms are either incomplete or preserved in a contorted orientation ( Fig. 4b, c ). All arms appear to have suckers along the base and midlength ( Fig. 4d ). The better-preserved shorter arms appear to show distal suckers; it is unclear if the elongated arms bear suckers distally ( Fig. 4d ). Suckers are commonly between ~0.31 and ~0.62 mm in diameter. Suckers appear to have been biserial wherever present, but both rows are not always preserved along the entire arm length. Sucker rows are laterally separated by ~0.5 mm ( Fig. 4e–g ). Within a row, suckers are immediately adjacent proximodistally or separated by up to ~0.4 mm ( Fig. 4e–g ). There is no evidence that suckers were stalked.

Most arms are incompletely preserved, so it is possible that the apparent elongation of two of the arms is a taphonomic artifact. We consider this unlikely because exactly two arms are elongated and the elongated arms are of approximately similar lengths, suggesting they are from the same arm pair. Furthermore, the better-preserved shorter arms are each of approximately similar lengths. Probability suggests a preservational artifact would result in a non-two number of unequally elongated arms associated with shortened arms of dissimilar lengths. Additional fossil specimens will be necessary to test this hypothesis though. Based on the phylogenetic affinity of Syllipsimopodi , we interpret these as arm pair II. However, precise arm identities cannot be determined; this is an inference not an observation. Syllipsimopodi bideni is conservatively coded unknown in the phylogenetic analysis for all characters related to the modification/elimination of arm pair II (Supplementary Data 1).

A possible funnel measuring ~2.4 mm long is preserved at the lateral edge of the head ( Fig. 3 ). Afunnel identification is advocated because suckers appear to be absent on the structure ( Fig. 4d ), and we cannot easily connect it to one of the ten identified arms ( Fig. 4b, c ).

The buccal apparatus is preserved as a dark rectangular patch within a light circular patch that is distinct from the surrounding arm/head tissues ( Fig. 3 , Supplementary Fig. 5 ). The dark structure (~3.5 × ~1.3 mm) appears to be texturally distinct from the other preserved tissues, suggesting it could be a remnant of the beak. An intriguing S-shaped band measuring ~0.33 mm in width is preserved within the buccal apparatus. It is possible that this band is a remnant of the radula, but we suspect it is more likely to be a superimposed sucker-bearing arm because of the relatively long length (in comparison to the dark rectangular patch) and the apparent circular shapes lining parts of the band.

A dark, contiguous, anteroposteriorly elongate, saclike structure is preserved laterally offset from the central median ridge of the gladius. We interpret this as the ink sac. The ink sac measures ~2.6 cm long anteroposteriorly and ~0.3 cm wide laterally at the widest point ( Figs. 3 , 4 ).

Ecological interpretations. The preserved soft tissues and gladius suggest a torpedo-shaped body reminiscent of extant squids. The fins appear to have been large enough to potentially function as a viable supplement to jet swimming, but their apparent circular shape and terminal position would seem to suggest a stabilizing role may have been more important. If the arms are preserved to approximately their total lengths, then one arm pair was considerably longer than the other four pairs, which were shorter (arm-to-body length ratio) than in most extant octobrachians37. It seems likely that the elongated arms captured prey to be confined and manipulated by the shorter arms, analogous to extant decabrachians. The type does not preserve identifiable gut contents, so diet is unknown. While Vampyroteuthis remains the best living analog for understanding extinct vampyropods (because it is the most plesiomorphic extant vampyropod), these observations suggest Syllipsimopodi may have filled a niche more similar to extant inshore squids, i.e., a midlevel nektic predator. It is not inconceivable that Syllipsimopodi may have used its suckerladen arms to pry small ammonoids out of their shells, or ventured more inshore to similarly extract small brachiopods, bivalves, and/or conulariids18,22; this is speculation though.

Remarks. There is considerable disagreement regarding the proper terminology for the group combining vampyromorphs, octopods, and their ancestors— Octobrachia, Octopodiformes, and Vampyropoda are the most common names. The Treatise on Invertebrate Paleontology 7 recommends Octobrachia as a superorder for all coleoids that have either lost appendage pair II or modified it into filaments (i.e., Prototeuthidina, Loligosepiina, Teudopseina , Vampyromorphida , and Octopoda ). We follow this recommendation ( Fig. 1 ) and thus consider Octobrachia to be an apomorphy-defined taxon. We suggest that the name Octopodiformes be retained for the crown group ( Fig. 1 ), since this appears to be the more popular term in the neontological literature. The name Vampyropoda, which is popular amongst paleontologists and has been formally ranked above Octobrachia 38, should be retained for the total group ( Fig. 1 ). This keeps the three most common terms accurate as typically used in the literature, and provides clade names necessary for greater nomenclatural precision, without inventing additional terms that would further confuse the discussion.

The Bayesian FBD (Fossilized Birth-Death) analysis reconstructs Syllipsimopodi bideni gen. et sp. nov. as the earliestdiverging vampyropod; the node is well supported with a posterior probability of 93% ( Fig. 6 ). This placement is supported by the loss of the phragmocone, loss of the primordial rostrum, presence of a median ventral interruption on the gladius/proostracum, and dorsal shell (Supplementary Fig. 8, Supplementary Notes). The Early Triassic Idahoteuthis, which had been described as a possible myopsid squid39, is also recovered as an early vampyropod; the node has a posterior probability of 99% ( Fig. 6 ). In addition to the characters shared with Syllipsimopodi , the position of Idahoteuthis is supported by the presence of lateral fields and the shape of the anterior median field (Supplementary Fig. 8, Supplementary Notes). Prototeuthidina is recovered as the earliest diverging octobrachian clade ( Figs. 1 , 6 ), unlike past parsimony analyses, which reconstructed the prototeuthids as derived loligosepiids1,2 or stem octopods2. These results better agree with recent non-cladistic arguments and the stratigraphic record – the oldest known octobrachians are the Triassic prototeuthids Germanoteuthis and Reitneriteuthis 7. Rather than the basalmost octobrachian1, the Jurassic Proteroctopus is recovered as the basalmost stem vampyromorph ( Figs. 1 , 6 ). Loligosepiina is recovered as a clade sister to Vampyromorphida ( Figs. 1 , 6 ); previous cladograms reconstructed the loligosepiids as either a grade of stem octopodiforms1 or a grade of stem octopods2. Vampyronassa and Leptoteuthis (formerly a loligosepiid7 but never cladistically positioned within the group1,2) are recovered as vampyromorphs ( Fig. 6 ).

Teudopseina is recovered as a paraphyletic grade of stem octopods ( Figs. 1 , 6 ). Past cladograms reconstructed them as total group vampyromorphs2, or as a combination of stem octopodiforms and stem octopods1; no phylogenies have recovered a monophyletic Teudopseina , Teudopseidae , or Teudopsis 1,2,40. We establish new genera for Teudopsis bollensis ( Briggsiteuthis gen. nov.), Teudopsis jeletzkyi ( Fuchsiteuthis gen. nov.), and Teudopsis subcostata ( Suttoniteuthis gen. nov.), which have each consistently been shown to be phylogenetically isolated from the type species, Teudopsis bunelii 1,2,38 ( Fig. 6 ). T. jeletzkyi and T. subcostata are not assigned the same genus because their clade ( Fig. 6 ) is not found in other phylogenies1,2. Teudopseina could be maintained as a monophyletic rump group by restricting the suborder to Teudopseidae and Palaeololiginidae ( Fig. 6 )—this clade has been recovered in all phylogenies1,2. All analyses also suggest Teudopseidae is fully (no rump group) paraphyletic1,2 or polyphyletic ( Fig. 6 ) with respect to Palaeololiginidae , which has nomenclatural seniority7, making Teudopseidae a junior synonym. The rump suborder Teudopseina would thus consist of one family, Paleololiginidae; we decline subordinal revision until interrelationships are more stable though. Unlike past studies1,2, we recover a monophyletic Trachyteuthidae ( Fig. 6 ). We establish new genera for the trachyteuthids Glyphiteuthis rhinophora ( Justinianiteuthis gen. nov.), Glyphiteuthis minor ( Fisheriteuthis gen. nov.), and Trachyteuthis bacchiai ( Edmunditeuthis gen. nov.) because each species has consistently been found isolated from its respective genus1,2 ( Fig. 6 ). The latter two species were not reassigned to Glyphidopsis because that clade ( Fig. 6 ) was not recovered in other phylogenies1,2. The Supplementary Discussion includes taxonomic details of the new genera.

We recovered belemnoid monophyly ( Fig. 6 ), as in past analyses1,2; however, our results place Belemnoidea sister to Decabrachia ( Fig. 1 ) rather than within Decabrachia, sister to Sepiida (cuttlefishes) and Sepiolida (bobtail squids)1,2. Our topology better concords with the stratigraphic record and molecular divergence time estimates. The oldest definitive fossil cuttlefish is the Maastrichtian Ceratisepia 41 but the oldest definitive belemnoid is the Changhsingian phragmoteuthid Permoteuthis 42. Both our morphological FBD tree ( Fig. 6 ) and molecular clock estimates suggest cuttlefish split from Spirula in the Jurassic43. For belemnoids to be included within Decabrachia, the sepiid-spirulid split would need to occur in the Palaeozoic.

Phragmoteuthids have long been viewed as a likely precursor to the gladius-bearing coleoids, and hence vampyropods44–46, but this narrative has been rejected by all cladistic analyses1,2 ( Fig. 6 ). Instead, phragmoteuthids consistently cluster with the other belemnoids and the belemnoids with decabrachians. Nevertheless, the idea has remained prominent in the literature4,42, in part because the tripartite phragmoteuthid proostracum seems reminiscent of vampyropod proostraca. This is explainable if lateral fields are a neocoleoid symplesiomorphy—meaning that either lateral fields were uniquely lost by Syllipsimopodi , or they were not well preserved in the Syllipsimopodi holotype (we could not conclusively determine presence/absence). Alternatively, the vampyropod lateral fields may have developed independently of comparable structures in belemnoids and decabrachians ( Fig. 6 ). Past cladistic analyses1,2 did not test the stratigraphic arguments for phragmoteuthid origins. Phragmoteuthids originated in the latest Permian (Changhsingian)42, and the oldest vampyropods had previously been known from no earlier than the Middle Triassic (Ladinian)7; a comfortable timeline for divergence. However, our FBD phylogeny explicitly incorporates stratigraphy and still rejects a phragmoteuthid origin for Vampyropoda. This is unsurprising as Syllipsimopodi predates all known phragmoteuthids by nearly 70 million years, and it already possessed a dorsal gladius without a phragmocone or primordial rostrum.

Spirulida is here recovered as the basalmost decabrachian order ( Fig. 6 ), but this may be biased by their plesiomorphic shellcondition. Nevertheless, results appear substantially more plausible than previous fossil-inclusive cladograms, which reconstructed spirulids as deeply nested within Decabrachia1,2. Molecular phylogenies have produced conflicting results for the position of Spirula , suggesting placement within Bathyteuthida47 or as sister to either Myopsida48, Oegopsida9,49, Bathyteuthida + Oegopsida50, or Sepiida 51. We recover Sepiida as the next earliest diverging order, and the teuthids (Myopsida, Bathyteuthida, and Oegopsida) are recovered in a clade sister to Idiosepiida + Sepiolida ( Fig. 6 ). Decabrachians were not a focus of this analysis though, and our limited sampling is not intended or expected to meaningfully resolve interrelationships within this group.

Figures

Fig. 3 Syllipsimopodi bideni gen. et sp. nov., holotype ROMIP 64897. a Schematic drawing of Syllipsimopodi bideni gen. et sp. nov.; teal = gladius, orange = head (including arms), brown = buccal apparatus, gray = ink sac, blue = conus, magenta = fin support, patterned yellow = scale-like patches (possible connective tissue remnant). b Increased contrast false color image of Syllipsimopodi, holotype ROMIP 64897. Scale = 1 cm. c Artistic reconstruction showing suckers (created by K. Whalen).

Fig. 4 Syllipsimopodi bideni gen. et sp. nov., holotype ROMIP 64897, showing arm crown. a–d Scale = 1 cm. a Complete body fossil. b–d Showing arm crown; c arm traces in blue, purple indicates the arm is overlapping below two other arms, green indicates the arm is overlapping above itself; d red and yellow circles mark individual suckers. e–g scale = 5 mm; closeup of arms showing suckers, select suckers indicated with white arrows.

Fig. 2 Idealized drawing of vampyropod gladius (based on Vampyroteuthis). Showing median field, hyperbolar zones, lateral fields, and cone flags, with examples of growth lines. Asymptotes denote borders of hyperbolar zones.

Fig. 5 Overview of coleoid shell evolution, showing our interpretations of the gladius/proostracum. Early coleoids, such as Gordoniconus13, add the primordial rostrum85 and proostracum14; vampyropods lose the phragmocone and primordial rostrum, the proostracum is now a gladius14; belemnoids and early decabrachians lose the body chamber86 and add the rostrum85; oegopsids lose the rostrum, some retain a demineralized primordial rostrum85 and phragmocone71, the proostracum is now a gladius14. Structures only labeled when they appear (solid black line) or are lost (dashed black line). Shell tissues: orange = phragmocone + body chamber (dashed = demineralized), blue = proostracum/gladius, green = primordial rostrum (dashed = demineralized), yellow = rostrum.

Fig. 1 Overview of neocoleoid interrelationships and divergence time estimates, showing the position of Syllipsimopodi bideni gen. et sp. nov. Based on our Bayesian tip-dated phylogenetic reconstruction (Fig. 6). Shells color coded: blue = proostracum/gladius (hyperbolar zones and lateral reinforcements in darker blue), orange = phragmocone, green = primordial rostrum, yellow = rostrum. Geologic period abbreviations (colors from International Commission on Stratigraphy): = Cambrian (dark green), O = Ordovician (teal), S = Silurian (light blue), D = Devonian (brown), C = Carboniferous (blue), P = Permian (red orange), TR = Triassic (purple), J = Jurassic (cyan), K = Cretaceous (green), PG = Paleogene (orange), N = Neogene (yellow), unlabeled = Quaternary (pale yellow). Purple arrows indicate named nodes, purple bar indicates teudopseid grade. Artistic depictions created by K. Whalen.

Fig. 6 Bayesian tip-dated FBD (Fossilized Birth-Death) morphological phylogeny of neocoleoid cephalopods, showing the position of Syllipsimopodi bideni gen. et sp. nov. Numbers at nodes indicate posterior probabilities (percentage). Tips dated from the first appearance of the oldest member of the relevant lineage in the fossil record (see “Methods” and Supplementary Information). Showing geological timescale dated using Gradstein et al.2, dates in Ma and colors from International Commission on Stratigraphy; Q = Quaternary (pale yellow). Important taxa highlighted: orange = Belemnoidea, purple = Decabrachia, yellow = Prototeuthidina, green = Loligosepiina, cyan = Vampyromorphida, blue = ‘teudopseid’ grade, red = Octopoda. Tree does not show revised taxonomic designations: Teudopsis bollensis = Briggsiteuthis bollensis gen. et comb. nov., Teudopsis jeletzkyi = Fuchsiteuthis jeletzkyi gen. et comb. nov., Teudopsis subcostata = Suttoniteuthis subcostata gen. et comb. nov., Glyphiteuthis rhinophora = Justinianiteuthis rhinophora gen. et comb. nov., Glyphiteuthis minor = Fisheriteuthis minor gen. et comb. nov., and Trachyteuthis bacchiai = Edmunditeuthis bacchiai gen. et comb. nov. Tree drawn from MrBayes TRE output file using icytree.org. Source data are provided as a Source data file.