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Cephalopod Mollusks (Cephalopoda)

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Cephalopod Mollusks (Cephalopoda) Cephalopod mollusks (Cephalopoda) Jan M. Strugnella,*, Annie Lindgrenb, and alternative classiA cations have been proposed for rela- A. Louise Allcockc tionships within Cephalopoda (2). Herein we follow the aDepartment of Zoology, University of Cambridge, Downing St, classiA cation of Young et al. (3) that generally does not Cambridge, CB2 3EJ, UK; bMuseum of Biological Diversity, The Ohio include ranks above the family level; however, we make c State University, 1315 Kinnear Road, Columbus, OH 43215, USA; The certain assumptions about rank based on nomenclature Martin Ryan Marine Science Institute, National University of Ireland and position. Galway, University Road, Galway, Ireland. *To whom correspondence should be addressed (jan.strugnell@ 7 e Coleoidea are divided into two superorders: gmail.com) Decapodiformes and Octopodiformes (4). 7 e Decapod- iformes is a morphologically and ecologically diverse group comprising 31 families, 95 genera, and approxi- Abstract mately 450 species. Four major lineages are recognized within Decapodiformes: Sepioidea (cuttleA sh, bottletail, Squids, cuttlefi sh, octopuses, and nautiluses (~700 species) and bobtail squids), Spirulida (the Ram’s horn squid), are grouped into 47 families within the Class Cephalopoda Oegopsida (open-eye squids), and Myopsida (closed- of the Phylum Mollusca. The resolution of many higher- eye squids) (3, 5). 7 ree families, Bathyteuthidae, level phylogenetic relationships within cephalopods has been hindered by homoplasy among morphological char- acters, although some recent progress has been made with molecular phylogenies and molecular clocks. The cephalo- pod timetree supports a Paleozoic (542–251 million years ago, Ma) origin of the Orders Vampyromorpha, Octopoda, and the majority of the extant higher-level decapodi- form taxa. The major lineages within the Order Octopoda were estimated to have diverged during the Mesozoic era (251–66 Ma). 7 e class Cephalopoda is a monophyletic group which can be divided into two subclasses; Nautiloidea and Coleoidea. Nautiloidea contains the nautiluses (Nautilus and Allonautilus), whereas Coleoidea contains the octo- puses (Fig. 1), squids, and cuttleA shes. Coleoid cepha- lopods diB er from nautiloids most notably through the reduction (or complete loss) and internalization of the shell. DeA ning features of Coleoidea include a muscular mantle used for locomotion and respiration, the modi- A cation of the foot into appendages around the mouth, a closed circulatory system, and complex eyes with lenses, although many of these features have been lost or reduced in various taxa. 7 e widely cited annotated classiA cation of the recent Cephalopoda (1) listed over 700 valid species in 139 genera and 47 families. Here we review the evolutionary relationships and divergence Fig. 1 A benthic octopus (Pareledone charcoti) from Antarctica. times of the members of the class Cephalopoda. Several Photo credit: A. L. Allcock. J. M. Strugnell, A. Lindgren, and A. L. Allcock. Cephalopod mollusks (Cephalopoda). Pp. 242–246 in e Timetree of Life, S. B. Hedges and S. Kumar, Eds. (Oxford University Press, 2009). HHedges.indbedges.indb 224242 11/28/2009/28/2009 11:27:04:27:04 PPMM Eukaryota; Metazoa; Mollusca; Cephalopoda 243 Sepiolidae 4 Sepiidae 8 3 Spirulidae Sepioidea Loliginidae 2 Ommastrephidae Myopsida 10 Joubiniteuthidae 7 1 Pyroteuthidae Decapodiformes 6 Oegopsida Bathyteuthidae Idiosepiidae D C P TrJ K Pg Ng PALEOZOIC MESOZOIC CZ 400 300 200 100 0 Million years ago Bolitaenidae 16 Vitreledonellidae 15 Octopodidae-3 Ctenoglossa 14 13 Octopodidae-2 Octopodidae-1 Incirrata 11 Tremoctopodidae Octopoda 12 9 Argonautidae Opisthoteuthidae Argonautoidea 5 17 Stauroteuthidae Cirrata Vampyroteuthidae P TriassicJurassic Cretaceous Pg Ng PZ MESOZOIC CENOZOIC 250 200 150 100 50 0 Million years ago Fig. 2 A timetree of cephalopod mollusks: Decapodiformes and Octopodiformes. Divergence times are shown in Table 1. Abbreviations: C (Carboniferous), CZ (Cenozoic), D (Devonian), J (Jurassic), K (Cretaceous), Ng (Neogene), P (Permian), Pg (Paleogene), PZ (Paleozoic), and Tr (Triassic). Octopodidae 1 = Octopus, Hapalochlaena; Octopodidae 2 = Benthoctopus, Enteroctopus; Octopodidae 3 = Adelieledone, Pareledone. Chtenopterygidae, and Idiosepiidae, have features that any modern phylogenetic study containing representa- do not clearly place them within one of these lineages. tives of each of these taxa. Some molecular studies sup- However, it appears that bathyteuthids and chtenop- port a relationship between Bathyteuthidae, Spirulida, terygids are closely related and these have been grouped and Sepioidea but not Idiosepiidae (14), while others together in the Bathyteuthoida (3). 7 e somewhat unique support a close relationship between Bathyteuthidae and pygmy squids (6), Idiosepiidae, currently remain as a Oegopsida (11). stand-alone family. Relationships among the lineages Sepioidea contains two groups, the bobtail squids, remain somewhat unclear due to conP icting or incon- Sepiolida (families Sepiolidae and Sepiadariidae), and clusive analyses of both morphological (7) and molecu- the cuttleA shes (Family Sepiidae), united by morpho- lar (8–11) data. Sepioidea, Idiosepiidae, and Spirulida logical features such as eyes with secondary lids and a have oJ en been interpreted as closely related (12, 13), funnel with a lateral canal (5). Molecular data have yet but have never been found to be a monophyletic group in to support a monophyletic Sepioidea; recent molecular HHedges.indbedges.indb 224343 11/28/2009/28/2009 11:27:08:27:08 PPMM 244 THE TIMETREE OF LIFE Table 1. Divergence times (Ma) and their credibility intervals corneal covering over the eye. 7 e absence of a cornea (CI) among cephalopod mollusks. implies either a close relationship with Oegopsida or that Timetree Estimates loss is a convergent character in Sepiidae and Oegopsida. Naef (12) believed Spirulida to be closest to Sepiidae Node Time Ref. (11)(a) Ref. (11)(b) (cuttleA shes) due to similarity in embryonic phragmo- Time CI Time CI cone development. Some molecular studies have found 1390.0390.0596–236– – a close relationship between Spirulida and Sepiidae (10, 2349.0349.0544–206– – 14), although other molecular studies (8, 9) yielded dif- 3321.0321.0506–188– – ferent phylogenetic positions for Spirulida. Because of 4297.0297.0473–172– – the unique morphological characters and inconsistent 5 285.5 252.0 369–175 319.0 476–206 results with DNA sequence data, further examination is required before the position of Spirulida can be A rmly 6282.0282.0454–161– – established. 7230.0230.0– – – Oegopsida and Myopsida were historically grouped 8206.0206.0345–109– – together in the Suborder Teuthoidea (e.g., 12), united by 9 195.5 174.0 262–118 217.0 336–133 similarities in gladius, branchial canal, tentacular clubs, 10175.0––––and interstellate connective (15). 7 e primary feature 11 156.0 136.0 208–92 176.0 277–106 used to separate Oegopsida and Myopsida is the lack of a 12 111.5 105.0 166–67 118.0 196–66 corneal covering in the oegopsid eye. A close relationship 13 110.0 100.0 155–66 120.0 196–70 between Myopsida and Oegopsida was found in several topologies generated by Carlini and Graves (8) using the 14 88.5 77.0 121–49 100.0 166–57 COI locus, but other analyses have rendered Oegopsida 15 77.5 67.0 107–43 88.0 146–50 paraphyletic with respect to Myopsida, or found a close 16 75.0 65.0 – 85.0 – relationship between Myopsida and some sepioids (9–11). 17 75.0 65.0 – 85.0 – Myopsida and Sepioidea exhibit several features in com- Note: Node times in the timetree represent the mean of time estimates mon, such as the presence of a cornea, beak without an from different studies. Divergence times for the Octopodiformes are from angled point, vena cava ventral to intestine, buccal crown a Bayesian analysis of (a) three mitochondrial and three nuclear genes with suckers (only some taxa), accessory nidamental partitioned by gene and codon and (b) three nuclear genes partitioned glands, and tentacle pockets (15). Because of the lack of by gene and codon. Divergence times for Decapodiformes are from a Bayesian analysis of (a) three nuclear genes not partitioned (fi rst and resolution at basal nodes in the tree, many of the features second codon positions only). that unite Sepioidea and Myopsida may be ancestral. 7 e lack of a consistent relationship between Myopsida and Oegopsida suggests that the taxon Teuthoidea may not be valid. studies found Sepiidae to be closest to Spirulida ( 10, Oegopsida is the most species-rich and morphologic- 14), with Sepiolidae closest to a Sepiidae + Spirulida ally diverse group within the Decapodiformes. Species clade. Alternatively, Lindgren et al. (9) found Sepiidae can range in size from a few centimeters in the Family and Idiosepiidae to be closest relatives, while Strugnell Pyroteuthidae to tens of meters in the giant squid, et al. (10, 11) found Idiosepiidae and Sepiolidae to be Architeuthis dux. 7 e diversity in anatomy, behavior, closest relatives. Although their relationships are some- and morphology of Oegopsida, combined with a some- what unstable across molecular analyses, Sepiidae and what uninformative fossil record (15), has made gener- Sepiolida appear to be closely related on the basis of both ating hypotheses of family-level relationships within morphological and molecular data. this group very di1 cult. Morphology-based phylogenies Spirulida contains a single living species, Spirula have focused primarily on higher-level relationships, spirula, which exhibits
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