The First Vampire (*squid): How a Ten-Armed Fossil Rewrote Octopus History

Abstract

The evolutionary history of the Cephalopoda has long been fragmented, split between the scant, soft-tissue fossils of the Paleozoic and the molecular inferences of modern genomics. For decades, the origin of the Octopodiformes—the lineage comprising octopuses and the enigmatic vampire squid—remained a chronological puzzle, with molecular clocks predicting a Carboniferous divergence that the fossil record failed to substantiate. The recent description of Syllipsimopodi bideni, a ten-armed vampyropod from the Mississippian Bear Gulch Lagerstätte, has radically recalibrated this timeline, anchoring the group’s origins 82 million years earlier than previously confirmed. Concurrently, the sequencing of the Vampyroteuthis infernalis genome has revealed a "genomic living fossil" that retains the ancestral chromosomal architecture of the coleoid stem. This report integrates paleontological morphometrics and deep-time genomics to reconstruct the vampyropod trajectory: a lineage that began as shallow-water, ten-armed predators before diverging into the morphologically plastic octopuses and the evolutionarily conservative, deep-sea vampire squids.

1. Introduction: The Ghost Lineage

In evolutionary biology, "ghost lineages" refer to organisms inferred to exist by phylogeny but missing from the fossil record. For the Vampyropoda (or Octopodiformes), this ghost period spanned tens of millions of years. While modern octopuses and vampire squids clearly shared a common ancestor, the oldest definitive fossils appeared only in the Triassic.¹ Yet, molecular clocks persistently suggested that the split between the ten-armed Decapodiformes (squids, cuttlefish) and the eight-armed Octopodiformes occurred much earlier, likely in the Paleozoic.²

The resolution to this paradox lay dormant in the collections of the Royal Ontario Museum for over thirty years. Specimen ROMIP 64897, a fossil unearthed in 1988 from Montana's Bear Gulch Limestone, was finally described in 2022 as Syllipsimopodi bideni.³ Dating to the Serpukhovian age of the Carboniferous (approx. 328 Ma), this specimen is not merely the oldest known vampyropod; it is a transitional mosaic. It possesses the gladius of a squid, the sucker-laden arms of an octopus, and—crucially—a count of ten functional appendages.³

When viewed alongside recent genomic breakthroughs—specifically the 2025 sequencing of the Vampyroteuthis infernalis genome—S. bideni allows us to triangulate the ancestral state of all modern coleoids. We can now trace a direct line from the sunlit bays of the Carboniferous to the oxygen-starved abyss of the modern ocean, revealing a story of genomic revolution in octopuses and stubborn stasis in their vampire cousins.

2. The Carboniferous Prologue: Syllipsimopodi bideni

2.1 The Bear Gulch Taphonomic Window

The preservation of Syllipsimopodi bideni is a result of the unique depositional environment of the Bear Gulch Lagerstätte. During the Serpukhovian, central Montana was a tropical bay situated near the paleo-equator.⁶ The basin was characterized by a specific hydrodynamic regime where monsoonal storms triggered microturbidites—cascades of fine-grained, organic-rich sediment—that rapidly buried benthic and nektonic life.⁸

Unlike typical anoxic preservation, the Bear Gulch geochemistry favored phosphatization. Phosphate drawn from decaying organic matter precipitated early in diagenesis, replacing soft tissues such as muscles and gills before bacterial decomposition could consume them.⁹ This process captured the delicate features of S. bideni that would otherwise vanish: the ink sac, the fins, and the micron-scale details of the arm suckers.¹⁰

2.2 Morphology of the Decabrachian Ancestor

The anatomy of S. bideni provides the first morphological proof that the ancestor of octopuses and vampire squids was decabrachian (ten-armed).

• Arm Crown: The specimen displays ten arms bearing biserial rows of suckers (two rows per arm).³ Measurements of the holotype reveal that two of these arms were elongated (~4.0 to 4.1 cm long) relative to the other eight, constituting roughly 27% of the total body length.¹¹ This elongation suggests that the differentiation of appendages into "arms" and "tentacles" (or filaments) began early in coleoid evolution.¹²

• Gladius and Shell Reduction: Unlike its belemnoid contemporaries, S. bideni lacked a chambered phragmocone (the buoyancy-controlling part of the shell). Instead, it possessed a simplified gladius—a flattened, chitinous internal support.³ This loss of the phragmocone is a synapomorphy (shared derived character) of the Vampyropoda, marking the transition from rigid, shelled buoyancy to the agile, muscular hydrostatics of modern cephalopods.¹³

• Ink Sac: The presence of a preserved ink sac is ecologically telling.⁴ It confirms that this ancestor inhabited the photic zone where visual predation was a selective pressure, a sharp contrast to the ink-less, deep-sea existence of its modern descendant, Vampyroteuthis.¹⁴

2.3 Taxonomic Contention: The Gordoniconus Debate

The description of S. bideni has not been without controversy. In 2023, paleontologist Christian Klug and colleagues challenged the validity of the genus, proposing it as a junior synonym of Gordoniconus beargulchensis, another coleoid from the same locality.¹¹ Klug et al. argued that the "ten arms" were taphonomic artifacts—displaced mantle tissue or arms split during fossilization—and that the "ink sac" was merely a preserved esophagus.¹⁵

However, the original authors, Whalen and Landman, maintain the distinctness of the taxon. They point to specific anatomical divergences: Gordoniconus possesses a septate phragmocone and a primordial rostrum, features definitively absent in Syllipsimopodi.¹⁶ Furthermore, the gladius of S. bideni exhibits a smooth, bipartite median rib, distinct from the complex median structure of Gordoniconus.¹⁷ The presence of suckers on all ten appendages in S. bideni further supports the functional reality of the decabrachian condition, reinforcing its position as the basal vampyropod.¹⁷

3. The Genomic Archive: Vampyroteuthis infernalis (the Vampire Squid)

While S. bideni anchors the lineage in deep time, the modern vampire squid, Vampyroteuthis infernalis, serves as a living archive of the lineage's genetic history. A 2025 study led by Oleg Simakov has decoded the Vampyroteuthis genome, revealing it to be as much a "living fossil" molecularly as it is morphologically.¹⁹

3.1 The Ancient Coleoid Chromosomal Rearrangement Event (ACCRE)

The Vampyroteuthis genome is colossal, spanning over 11 billion base pairs.²¹ Despite this expansion, its architecture is remarkably conservative. The study identified traces of an "Ancient Coleoid Chromosomal Rearrangement Event" (ACCRE)—a major genomic reorganization that occurred in the common ancestor of all coleoids.²²

Critically, Vampyroteuthis has preserved the chromosomal synteny (gene order) established after this event. It retains a karyotype of approximately 46 chromosomes, a number shared with modern Decapodiformes (squids).²³ This confirms that the ancestral vampyropod was genetically "squid-like," possessing a high chromosome count that would later be drastically reduced in the octopus lineage.²⁴

3.2 Fusion-with-Mixing: The Mechanism of Octopus Innovation

The divergence of the Octopoda from the vampire squid lineage was driven by a mechanism termed "Fusion-with-Mixing" (FWM).²²

• Fusion: In the lineage leading to modern octopuses, the ancestral 46 chromosomes underwent massive fusions, reducing the karyotype to roughly 30 chromosomes.²³

• Mixing: These fusions were followed by extensive inter-chromosomal translocations, which scrambled the gene order. This "mixing" brought regulatory elements and genes into new proximities, creating novel gene regulatory networks.²²

This genomic restructuring is hypothesized to be the engine of octopus complexity. The expansion of specific gene families, such as Protocadherins (cell adhesion molecules involved in neural development) and G-protein coupled receptors (GPCRs), is notably prevalent in octopuses but absent or reduced in Vampyroteuthis.²³ The explosive radiation of these gene families in octopuses correlates with their elaborate nervous systems, camera-like eyes, and complex behaviors. Vampyroteuthis, by bypassing this FWM event, retained a simpler neural architecture and the ancestral genomic layout.¹⁹

Table 1: Comparative Traits of the Vampyropod Lineage

Feature	Syllipsimopodi bideni (Carboniferous)	Vampyroteuthis infernalis (Modern)	Octopoda (Modern)
Divergence Time	~328 Ma (Stem)	~183 Ma (Crown origins)	~270 Ma (Split from stem)
Arm Count	10 (2 elongated)	8 + 2 Filaments	8 (2nd pair lost)
Sucker Morphology	Biserial, non-stalked	Uniserial (distal), cirri present	Biserial or Uniserial
Shell	Gladius (internal)	Gladius (broad, uncalcified)	Vestigial stylets
Genome Architecture	Unknown	Conserved (46 chrom.), Stasis	Derived (30 chrom.), Fusion-with-Mixing
Key Gene Families	Unknown	Ancestral Baselines	Expanded Protocadherins & GPCRs
Habitat	Shallow Tropical Bay	Deep Sea (OMZ)	Ubiquitous (Benthic/Pelagic)
Defense	Ink Sac	Bioluminescence (Ink Sac lost)	Ink Sac & Camouflage

4. Ecological Descent: Into the Abyss

The transition from the morphology of S. bideni to that of V. infernalis tells a story of ecological retreat and adaptation. S. bideni was a visual predator in shallow, illuminated waters, utilizing its ink sac to evade other predators.⁴

However, the Mesozoic Marine Revolution brought intensified competition from new predators, including advanced bony fishes and marine reptiles. The fossil record suggests that vampyromorphs began a vertical migration into deeper waters as early as the Jurassic or Oligocene.²⁸ Fossils like Simoniteuthis (Jurassic) and Necroteuthis (Oligocene) mark the steps of this descent.²⁹

In the bathypelagic zone, particularly the Oxygen Minimum Zone (OMZ), the selective pressures shifted.

• Loss of Ink: In the perpetual dark, ink is ineffective. Vampyroteuthis lost the ink sac and evolved bioluminescent organs for defense and communication.¹⁴

• Metabolic Slowdown: To survive in hypoxic conditions, the lineage evolved the lowest mass-specific metabolic rate of any cephalopod.³¹

• Feeding Shift: The predatory grasping arms of S. bideni were modified. One pair became sensory filaments for detecting "marine snow" (detritus), and the remaining arms became webbed for enveloping this passive food source, transforming the lineage from active hunters to energy-efficient scavengers.³²

5. Conclusion

The discovery of Syllipsimopodi bideni and the sequencing of the Vampyroteuthis genome provide a unified theory of vampyropod evolution. S. bideni is the "missing link" that confirms the decabrachian ancestry of the group, bridging the gap between the Paleozoic and the Mesozoic. It validates the molecular clock predictions that the lineage is far older than the Triassic fossils previously suggested.

Simultaneously, the Vampyroteuthis genome reveals the mechanism of this evolutionary divergence. While the octopus lineage underwent a chaotic "Fusion-with-Mixing" event that scrambled their chromosomes and fueled the evolution of complex neural traits, the vampire squid lineage remained genetically static. It retreated into the deep sea, preserving the ancestral coleoid genome and the ten-armed morphology (albeit modified) as a living archive of the Carboniferous.

Together, these findings depict a lineage that split strategy: one branch (octopuses) embraced genomic chaos and morphological reduction to conquer the shallow seas, while the other (vampire squids) embraced stasis and solitude, carrying the ghost of Syllipsimopodi into the dark safety of the abyss.

Works cited

1. Meet the ten-armed, 325-million-year-old octopus fossil named after President Joe Biden, accessed December 1, 2025, https://bigthink.com/life/ten-armed-octopus-named-after-biden/

2. Molecular clocks indicate turnover and diversification of modern coleoid cephalopods during the Mesozoic Marine Revolution | Proceedings of the Royal Society B: Biological Sciences - Journals, accessed December 1, 2025, https://royalsocietypublishing.org/doi/10.1098/rspb.2016.2818

3. Hail to the squid — A vampyropod fit for a president | Yale News, accessed December 1, 2025, https://news.yale.edu/2022/03/08/hail-squid-vampyropod-fit-president

4. Ancient Ten-Armed Octopus Relative Named for Joe Biden - Smithsonian Magazine, accessed December 1, 2025, https://www.smithsonianmag.com/smart-news/ancient-10-armed-octopus-relative-named-for-joe-biden-180979698/

5. Fossil coleoid cephalopod from the Mississippian Bear Gulch Lagerstätte sheds light on early vampyropod evolution - PubMed, accessed December 1, 2025, https://pubmed.ncbi.nlm.nih.gov/35260548/

6. Carboniferous Vampire-Squid-Like Cephalopod Had Ten Arms | Sci.News, accessed December 1, 2025, https://www.sci.news/paleontology/syllipsimopodi-bideni-10605.html

7. Paleontologists Just Discovered The Oldest-Known Octopus Ancestor — And It Predates Even The Dinosaurs - All That's Interesting, accessed December 1, 2025, https://allthatsinteresting.com/syllipsimopodi-bideni

8. The geological and biological environment of the Bear Gulch Limestone (Mississippian of Montana, USA) and a model for its deposition, accessed December 1, 2025, https://sciencepress.mnhn.fr/sites/default/files/articles/pdf/g2002n2a2.pdf

9. Fossil Lagerstätten and the enigma of anactualistic fossil preservation | Paleobiology, accessed December 1, 2025, https://www.cambridge.org/core/journals/paleobiology/article/fossil-lagerstatten-and-the-enigma-of-anactualistic-fossil-preservation/67C1279E3439E95FD77BAB35BA6B2E8A

10. Fossils and Their Preservation, accessed December 1, 2025, https://people.hws.edu/kendrick/paleontology/labs/lab01.html

11. Syllipsimopodi - Wikipedia, accessed December 1, 2025, https://en.wikipedia.org/wiki/Syllipsimopodi

12. Study: Octopus Ancestors Had 10 Arms - American Museum of Natural History, accessed December 1, 2025, https://www.amnh.org/explore/news-blogs/fossil-octopus-ancestor-arms

13. [Paleontology • 2022] Syllipsimopodi bideni • Fossil Coleoid Cephalopod (Cephalopoda: Coleoidea) from the Mississippian Bear Gulch Lagerstätte sheds light on early Vampyropod Evolution - Species New to Science, accessed December 1, 2025, http://novataxa.blogspot.com/2022/03/syllipsimopodi.html

14. Vampyroteuthis infernalis | INFORMATION - Animal Diversity Web, accessed December 1, 2025, https://animaldiversity.org/accounts/Vampyroteuthis_infernalis/

15. Revisiting the identification of Syllipsimopodi bideni and timing of the decabrachian-octobrachian divergence - PMC - NIH, accessed December 1, 2025, https://pmc.ncbi.nlm.nih.gov/articles/PMC10703834/

16. Part of a structure previously interpreted as a tentacle of... - ResearchGate, accessed December 1, 2025, https://www.researchgate.net/figure/Part-of-a-structure-previously-interpreted-as-a-tentacle-of-Gordoniconus-beargulchensis_fig5_334806320

17. (PDF) Reply to: Revisiting the identification of Syllipsimopodi bideni and timing of the decabrachian-octobrachian divergence - ResearchGate, accessed December 1, 2025, https://www.researchgate.net/publication/376453655_Reply_to_Revisiting_the_identification_of_Syllipsimopodi_bideni_and_timing_of_the_decabrachian-octobrachian_divergence

18. Reply to: Revisiting the identification of Syllipsimopodi bideni and timing of the decabrachian-octobrachian divergence - PMC - PubMed Central, accessed December 1, 2025, https://pmc.ncbi.nlm.nih.gov/articles/PMC10716472/

19. Vampires in the Deep: An Ancient Link Between Octopuses and Squids - Universität Wien, accessed December 1, 2025, https://www.univie.ac.at/en/news/detail/vampires-in-the-deep-an-ancient-link-between-octopuses-and-squids

20. Scientists Sequence Genome of Vampire Squid | Sci.News, accessed December 1, 2025, https://www.sci.news/genetics/vampire-squid-genome-14383.html

21. 'Vampire Squid From Hell' Reveals The Ancient Origins of Octopuses - Science Alert, accessed December 1, 2025, https://www.sciencealert.com/vampire-squid-from-hell-reveals-the-ancient-origins-of-octopuses

22. Chromosomal fusions and subsequent rearrangements shaped octopus genomes - bioRxiv, accessed December 1, 2025, https://www.biorxiv.org/content/10.1101/2025.05.16.652989v1.full-text

23. Giant genome of the vampire squid reveals the derived state of modern octopod karyotypes, accessed December 1, 2025, https://www.biorxiv.org/content/10.1101/2025.05.16.652989v2.full-text

24. Vampires in the deep: An ancient link between octopuses and squids | EurekAlert!, accessed December 1, 2025, https://www.eurekalert.org/news-releases/1107329

25. Chromosomal fusions and subsequent rearrangements shaped octopus genomes, accessed December 1, 2025, https://www.researchgate.net/publication/391842856_Chromosomal_fusions_and_subsequent_rearrangements_shaped_octopus_genomes

26. The gold-ringed octopus (Amphioctopus fangsiao) genome and cerebral single-nucleus transcriptomes provide insights into the evolution of karyotype and neural novelties, accessed December 1, 2025, https://pmc.ncbi.nlm.nih.gov/articles/PMC9795677/

27. Syllipsimopodi Bideni: An Octopus With 10 Arms Pushes Back The Age Of Vampyropoda By Nearly 82 Million Years | Science 2.0, accessed December 1, 2025, http://www.science20.com/news_staff/syllipsimopodi_bideni_an_octopus_with_10_arms_pushes_back_the_age_of_vampyropoda_by_nearly_82_million_years-255977

28. Ancient Origins of the Vampire Squid | Deep Sea News, accessed December 1, 2025, https://deepseanews.com/2024/03/ancient-origins-of-the-vampire-squid/

29. Fossil evidence for vampire squid inhabiting oxygen-depleted ocean zones since at least the Oligocene - ResearchGate, accessed December 1, 2025, https://www.researchgate.net/publication/349412571_Fossil_evidence_for_vampire_squid_inhabiting_oxygen-depleted_ocean_zones_since_at_least_the_Oligocene

30. A new vampyromorph species from the Middle Jurassic La Voulte‐sur‐Rhône Lagerstätte, accessed December 1, 2025, https://www.researchgate.net/publication/371844808_A_new_vampyromorph_species_from_the_Middle_Jurassic_La_Voulte-sur-Rhone_Lagerstatte

31. Vampire squid - Wikipedia, accessed December 1, 2025, https://en.wikipedia.org/wiki/Vampire_squid

32. MBARI researchers discover what vampire squids eat (it's not what you think), accessed December 1, 2025, https://www.mbari.org/news/mbari-researchers-discover-what-vampire-squids-eat-its-not-what-you-think/