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The evolution of Cephalopods and their present biodiversity and ecology
Abstract
The present status of phylogeny and classification in coleoid cephalopods and the effect of evolution on the present ecology and biodiversity in the group are examined. The basis of knowledge of cephalopod phylogeny was formulated by Naef in the early 1920s, and his ideas and the progress made in the intervening 75 years are investigated. In the process, the roles that transitions between pelagic and benthic habitats played in the evolution of cephalopods are noted, and the possibility is advanced that the most recent "oceanic anoxic event" may have established a time marker for the divergence of some oegopsid families. The major advances since Naef's work are: 1. The unusual nature of Vampyroteuthis has been recognized; 2. The sister-group relationship between the Neocoleoidea and the Belemnoidea has been established, but requires further confirmation; 3. Monophyly has been confirmed for the Decapodiformes (new name), Octopodiformes and Octopoda by molecular and morphological methodologies; 4. The dates of origin of the Belemnoidea, Neocoleoidea, Sepioidea and fossil teuthoids have been extended to considerably earlier times. The major unsolved phylogenetic problems in need of immediate attention are the position of the Myopsida, relationships within the Sepioidea, the identification of the basal nodes within the Oegopsida, and the relationships of most "fossil teuthoids."
... Modern coleoids possess several synapomorphic features, such as an internally shelled (endocochleate) body plan, one pair of gills, a complex nervous system with a central brain, image-forming eyes with lenses, and an ink sac, all of which allow living animals to acquire vertebrate-like intelligence (Nixon and Young, 2003). They are currently classified into two superorders, Decapodiformes Young, Vecchione and Donovan, 1998, comprising squids and cuttlefish with ten arms whose fourth pair is modified as tentacles; and Octopodiformes Berthold and Engeser, 1987, comprising octopuses and vampire squid (Vampyroteuthis infernalis) with eight arms (Doyle et al., 1994;Young et al., 1998;Lindgren, 2010). Available fossil data suggest that Coleoidea was derived from the extinct order Bactritida with an external orthoconic shell in the Early Carboniferous (Kr€ oger et al., 2011;Klug et al., 2019), and that the calcified internal chambered shell occupied by the coleoid crown group was reduced to a chitinous gladius and pen and/or largely lost in many groups during their evolutionary history (Donovan, 1977;Doyle et al., 1994;Kr€ oger et al., 2011;. ...
... Modern coleoids possess several synapomorphic features, such as an internally shelled (endocochleate) body plan, one pair of gills, a complex nervous system with a central brain, image-forming eyes with lenses, and an ink sac, all of which allow living animals to acquire vertebrate-like intelligence (Nixon and Young, 2003). They are currently classified into two superorders, Decapodiformes Young, Vecchione and Donovan, 1998, comprising squids and cuttlefish with ten arms whose fourth pair is modified as tentacles; and Octopodiformes Berthold and Engeser, 1987, comprising octopuses and vampire squid (Vampyroteuthis infernalis) with eight arms (Doyle et al., 1994;Young et al., 1998;Lindgren, 2010). Available fossil data suggest that Coleoidea was derived from the extinct order Bactritida with an external orthoconic shell in the Early Carboniferous (Kr€ oger et al., 2011;Klug et al., 2019), and that the calcified internal chambered shell occupied by the coleoid crown group was reduced to a chitinous gladius and pen and/or largely lost in many groups during their evolutionary history (Donovan, 1977;Doyle et al., 1994;Kr€ oger et al., 2011;. ...
Two lower jaws and one upper jaw of coleoid cephalopods recovered from the Santonian to lower Campanian (Upper Cretaceous) strata in Hokkaido, Japan were studied taxonomically. A comparison of the jaws of modern and fossil coleoids suggests that the two lower jaws are conspecific with the co-occurring non-belemnitid coleoid Longibelus matsumotoi represented by longiconic phragmocones. We designated them as L. matsumotoi (?) with reservations. The similarity between the lower jaws of L. matsumotoi (?) and the extant ram's horn squid Spirula spirula (order Spirulida) supports the evolutionary scenario from Longibelus to Decapodiformes, including spirulid Groenlandibelidae, which ranged
from the late Campanian to the late Maastrichtian. The other incomplete but very large upper jaw lacking the posterior part of the inner lamella was identified as Oegopsida, family, genus, and species indeterminate, with a long rostrum terminated at a sharply pointed tip in the outer lamella, as observed in the upper jaws of some extant species of this order. The extremely large oegopsid jaws described in this study and in our other papers from the SantonianeCampanian of Hokkaido provide a reliable fossil
record to infer the evolutionary history of this order.
... They are characterized by the presence of paired cirri along a single series of arm suckers, and paired fins supported by a cartilaginous internal shell (Voss, 1988, Collins andVillanueva, 2006). Morphologically, cirrates are considered to be primitive (Young et al., 1998). ...
Phylogenies for Octopoda have, until now, been based on morphological characters or a few genes. Here we provide the complete mitogenomes and the nuclear 18S and 28S ribosomal genes of twenty Octopoda specimens, comprising 18 species of Cirrata and Incirrata, representing 13 genera and all five putative families of Cirrata (Cirroctopodidae, Cirroteuthidae, Grimpoteuthidae, Opisthoteuthidae and Stauroteuthidae) and six families of Incirrata (Amphitretidae, Argonautidae, Bathypolypodidae, Eledonidae, Enteroctopodidae, and Megaleledonidae) which were assembled using genome skimming. Phylogenetic trees were built using Maximum Likelihood and Bayesian Inference with several alignment matrices. All mitochondrial genomes had the 'typical' genome composition and gene order previously reported for octopodiforms, except Bathypolypus ergasticus, which appears to lack ND5, two tRNA genes that flank ND5 and two other tRNA genes. Argonautoidea was revealed as sister to Octopodidae by the mitochondrial protein-coding gene dataset, however, it was recovered as sister to all other incirrate octopods with strong support in an analysis using nuclear rRNA genes. Within Cirrata, our study supports two existing classifications suggesting neither is likely in conflict with the true evolutionary history of the suborder. Genome skimming is useful in the analysis of phylogenetic relationships within Octopoda; inclusion of both mitochondrial and nuclear data may be key.
... Transcriptome data generated in this study for S. spirula provide additional evidence that Spirulida is more closely related to the oceanic oegopsid squids than to the nearshore, demersal/benthic decapodiforms (Sepiida, Idiosepiida, Sepiolida, Myopsida). Furthermore, a close relationship of S. spirula plus oegopsids with myopsids and sepiids provides further support for the hypothesis that decapodiforms evolved from an ancestral, benthic lifestyle to a derived oceanic lifestyle (e.g., Fuchs & Iba, 2015;Young et al., 1998). One issue with this "nearshore to offshore evolution" hypothesis is the presence of a belemnoid-like chambered shell (phragmocone) in S. spirula. ...
The molluscan clade Decapodiformes (Cephalopoda) comprises a diverse and enigmatic assemblage including inshore and offshore squids, bobtails, cuttlefishes, and the ram’s horn squid (Spirulida: Spirula spirula). The latter species is of particular interest to paleontologists because it is the only living cephalopod with an internal chambered, spiral-shaped, calcareous shell resembling those seen in some fossil cephalopod taxa. Spirulida has been difficult to place phylogenetically, in part because it shares different features with sepiolids, sepiids, and oegopsids, creating conflict in morphological analyses. Unlike morphological assumptions of a close relationship with sepiids, previous molecular studies have found support for Spirulida as a close relative of Bathyteuthida and Oegopsida. Identifying the correct phylogenetic placement of Spirulida could allow alternative hypotheses of phragmocone evolution, e.g., retention of an ancestral phragmocone in Spirulida and Sepiida vs. independent reacquisition of the phragmocone in these taxa, to be evaluated. In the present study, we combined new, high-quality transcriptome data for a specimen of Spirula spirula with additional new and previously published transcriptome data for decapodiform cephalopods. Phylogenetic analyses of several matrices yielded trees in which Spirula spirula was recovered as the sister group of the oceanic open-eyed squids (Oegopsida). This close relationship of Spirula to oceanic squids, rather than to nearshore, demersal/benthic decapodiform lineages, provides further support for an “onshore to offshore” model of decapodiform evolution.
... It appears to offer a setting suitable for nautiloids-tropical archipelagoes with scleractinian reefs in close proximity to deep ocean basins, and lacking pinnipeds save for the late Pleistocene monk seal (Rule et al., 2020)-yet, there are no records of nautiloids (except Aturia) from this area after the middle Eocene (Table S2) Edinger & Risk, 1994), but these events post-date the late Eocene disappearance of nautiloids from the Caribbean region. The absence of nautilids from the American Pacific coasts and dispersal barriers between the Caribbean region and the European Tethys, such as temperature and depths (as outlined for cuttlefish, cf., Young et al., 1998), could have prevented nautilids from re-colonizing the Caribbean region after their late Eocene disappearance. ...
Aim
Nautilus and Allonautilus , last members of the once widespread nautiloid cephalopods, are today restricted to the deep central Indo‐West Pacific Ocean, for reasons that remain unclear. Cephalopod evolution is generally considered as being driven by vertebrate predation; therefore, we investigated the role of whales and seals in the decline of nautiloids through the Cenozoic.
Location
Global.
Taxon
Nautiloids, pinnipeds, cetaceans.
Methods
Distribution data for nautiloids, pinnipeds and cetaceans through the Cenozoic were compiled and plotted on a series of paleogeographic maps. Nautiloid shell sizes were compiled and plotted against the first appearance of pinnipeds and cetaceans in key regions.
Results
From the Oligocene onward, nautiloids became extinct in areas where pinnipeds appeared. The exception is the agile nautiloid Aturia , extinct globally at the end of the Miocene. A major role of odontocetes in the demise of nautiloids is not apparent, except for a few brevirostrine Oligocene taxa from the North American Atlantic and Pacific coasts, which appeared in these areas at the same time as nautilids disappeared. The Oligocene disappearance of nautiloids (except Aturia ) from the American Pacific coasts coincides with the development of oxygen minimum zones (OMZs) in this region.
Main conclusions
We hypothesize that the Cenozoic spread of pinnipeds drove nautiloids into their present‐day central Indo‐West Pacific refuge. Additional factors for the local extinction of nautiloids in the Oligocene include predation by short‐snouted whales and the development of OMZs, preventing nautiloids from retreating into deeper water.
... Extant V. infernalis lack decabrachian-like stalks 2,18 and the neck of the attachment joins to the base of the acetabulum (Fig. 3c, and Supplementary Fig. 4), rather than being inserted into it 18 . The infundibulum is not distinct, and the suckers do not provide strong suction 27 . ...
Although soft tissues of coleoid cephalopods record key evolutionary adaptations, they are rarely preserved in the fossil record. This prevents meaningful comparative analyses between extant and fossil forms, as well as the development of a relative timescale for morphological innovations. However, unique 3-D soft tissue preservation of Vampyronassa rhodanica (Vampyromorpha) from the Jurassic Lagerstätte of La Voulte-sur-Rhône (Ardèche, France) provides unparalleled opportunities for the observation of these tissues in the oldest likely relative of extant Vampyroteuthis infernalis. Synchrotron X-ray microtomography and reconstruction of V. rhodanica allowed, for the first time, a high-resolution re-examination of external and internal morphology, and comparison with other fossil and extant species, including V. infernalis. The new data obtained demonstrate that some key V. infernalis characters, such as its unique type of sucker attachment, were already present in Jurassic taxa. Nonetheless, compared with the extant form, which is considered to be an opportunistic detritivore and zooplanktivore, many characters in V. rhodanica indicate a pelagic predatory lifestyle. The contrast in trophic niches between the two taxa is consistent with the hypothesis that these forms diversified in continental shelf environments prior to the appearance of adaptations in the Oligocene leading to their modern deep-sea mode of life.
... related Spirulida 11,12 . The siphuncle of the former is restricted to a series of organic membranes placed posteriorly of the chambers, whereas in the Spirulida it is formed by apicalward tubular extensions of the septa. ...
The coleoid cephalopod Spirula spirula , the only present-day representative of the coleoid order Spirulida, secretes a coiled shell consisting of a series of chambers divided by septa and connected by a siphuncle. It is the shell closest to those of ectochleate cephalopods: nautiloids, ammonoids. Therefore, its study is crucial in understanding the transformations that took place during the emergence of endocochleates. In this study, we have carried out detailed observations on the different structures composing the Spirula shell, with the aim of reconstructing their morphology, distribution, and mutual relationships. Alongside this, we also review the previous profuse terminology. Taking into account the additional information provided by growth lines and crystal orientations, we propose mechanisms for the secretion of the shell structures. All these mechanisms are integrated in a consistent way into a general model of chamber formation. The periostracum is secreted within a distinct periostracal groove. The outer shell layer is secreted externally to the periostracum by the soft tissues lining the shell externally. The internal shell layer is produced by the shell wall mantle, whereas the septa and the siphuncle are made periodically by a differentiated septal/siphuncular mantle. The most adoral septal mantle edge changes from secreting septal to internal shell wall material to produce the mural flap. The adapical ridge is formed by passive precipitates from cameral fluid residues trapped by surface tension, whereas the fibrous-prismatic deposits of the connecting ring are biominerals produced remotely within mantle secretions.
... Coleoids are common components of the mesopelagic community 15,16 , with the ca. 326 million year-old fossil record 17 suggesting ample time for parasites to have optimized their infection strategies. Of the few cephalopods studied (i.e. less than twenty-five percent of all species described), almost all mature individuals were shown to possess some sort of parasitic symbiont 18,19 . ...
Gill parasites of coleoid cephalopods are frequently observed during remotely operated vehicle (ROV) dives in the Monterey Submarine Canyon. However, little knowledge exists on the identity of the parasite species or their effects on the cephalopod community. With the help of ROV-collected specimens and in situ footage from the past 27 years, we report on their identity, prevalence and potential infection strategy. Gill parasites were genetically and morphologically identified from collected specimens of Chiroteuthis calyx, Vampyroteuthis infernalis and Gonatus spp. In situ prevalence was estimated from video footage for C. calyx, Galiteuthis spp., Taonius spp. and Japetella diaphana, enabled by their transparent mantle tissue. The most common parasite was identified as Hochbergia cf. moroteuthensis, a protist of unresolved taxonomic ranking. We provide the first molecular data for this parasite and show a sister group relationship to the dinoflagellate genus Oodinium. Hochbergia cf. moroteuthensis was most commonly observed in adult individuals of all species and was sighted year round over the analyzed time period. In situ prevalence was highest in C. calyx (75%), followed by Galiteuthis spp. (29%), Taonius spp. (27%) and J. diaphana (7%). A second parasite, not seen on the in situ footage, but occurring within the gills of Gonatus berryi and Vampyroteuthis infernalis, could not be found in the literature or be identified through DNA barcoding. The need for further investigation is highlighted, making this study a starting point for unravelling ecological implications of the cephalopod-gill-parasite system in deep pelagic waters.
Eight coleoid genera have so far been described from the Callovian‐aged La Voulte‐sur‐Rhône Lagerstätte ( c . 165 Ma; Ardèche, France), a locality noted for its unique three‐dimensional preservation of soft tissues. Here, we used high resolution x‐ray‐based imaging methods, in conjunction with reflectance transformation imaging, to study the soft tissues of a previously undescribed coleoid from the La Voulte‐sur‐Rhône locality. This analysis identified both an ink sac and internal light organs, a combination of defence mechanisms present in the Recent, although not previously described from the coleoid fossil record, as well as the presence of Octobrachia‐type arm musculature and Vampyroteuthis ‐like sucker attachments. The morphology of the gladius could not be attributed to any known coleoids and therefore justified the assignment of this single specimen to a new taxon: Vampyrofugiens atramentum . The addition of this new vampyromorph species not only increases the coleoid diversity known from the site, but also broadens the morphological variation observed in the co‐occurring coleoid taxa. These findings suggest that there was a high diversity of cephalopods occupying differentiated communities during the Middle Jurassic.
Based on a comprehensive analysis of molecular sequence data, the Sepiidae genera Acanthosepion Rochebrune, 1884; Ascarosepion Rochebrune, 1884; Aurosepina Jothinayagam, 1987; Decorisepia Iredale, 1926; Doratosepion Rochebrune, 1884; Rhombosepion Rochebrune, 1884 and Spathidosepion Rochebrune, 1884 are here re-instated and formally recognised as valid. Sepia Linnaeus, 1758 and Sepiella Gray, 1849 are retained, but Metasepia Hoyle, 1885 is placed in alternative combination with Ascarosepion. The subgenus Digitosepia Lipiński, 2020 is well supported and is herein elevated to generic status. Sepia trygonina (Rochebrune, 1884) and Sepia hieronis (Robson, 1924) are placed in new monotypic genera Erythalassa gen. nov. and Lusepia gen. nov. respectively. Hemisepius Steenstrup, 1875, also monotypic, is recognised as valid based on a unique synapomorphy: the presence of a fleshy ridge on each side of the antero-ventral mantle that bears a longitudinal row of black pores, however, H. typicus Steenstrup, 1875, was not included in our molecular analysis as tissue samples could not be obtained. Sepia tuberculata Lamarck, 1798, the type species for the nominal genus Spathidosepion, was not included for the same reason. Based on the morphological similarity between S. tuberculata and the sequenced taxa, S. papillata Quoy & Gaimard, 1832 and S. angulata Roeleveld, 1972 we tentatively assign these two taxa to Spathidosepion pending future confirmation. Where possible, each genus is diagnosed based on a combination of morphological and molecular characters.
Cirrate octopods swim by a combination of fin action and medusoid propulsion by the arm/web complex. The fins of cirrate octopods are associated with a unique cartilage-like shell in a shell sac. In cross-section, the fins have distinct proximal and distal regions, both of which are covered by a thin surface sheath of muscle. The distal region is characterized by dorsal and ventral layers of muscle somewhat similar to a typical decapod fin. In the proximal region, the fin cartilage forms a flat central core within the fin and provides skeletal support for attachment of densely packed muscle. Whereas Stauroteuthis maneuvers slowly by sculling with the fins, Grimpoteuthis swims primarily using powerful fin strokes. In Stauroteuthis, the mantle is extensively modified. The mantle opening closely surrounds the funnel, and the posterior mantle muscle is thickened and probably controls water flow for respiration. The "secondary web" in some cirrate species results from a modification of the way the web muscles attach to the arms. The more benthic opisthoteuthids lack this modification. The secondary web enables larger volumes of water to be trapped in the web in some postures. The entrapment of water resulting in a bell-shaped posture in Stauroteuthis could be related to predator defense or to feeding. Buccal secretory glands found in Stauroteuthis and the presence of small copepods in the digestive tract, suggest that this benthopelagic species feeds by entrapping planktonic prey in mucus.
Cephalopod taxonomy is still uncertain, and little is known of the phylogeny of Recent taxa. Biochemical and molecular characters are complementary to morphology, and allow an additional insight into the phylogenetic relationships among cephalopods. Eye lens protein electrophoresis and immunological approaches yield data in agreement with traditional taxonomic grouping, but are less suitable for establishing phylogenetic relationships. Molecular tools, e. g. the 3' end of the 16S rDNA gene, have failed to resolve the phylogeny at the suprafamilial level, but seem appropriate at lower levels. DNA sequence comparisons (% substitution) show that a direct relationship between taxonomic rank and nucleotide divergence cannot be established, as the nucleotide divergence level differs from one taxa to the other. Electrophoretic and immunological analyses of eye lens proteins as well as molecular results suggest that sepiolids should be separated from Sepioidea.
