Molecular clocks indicate turnover and diversification of modern coleoid cephalopods during the Mesozoic Marine Revolution

Abstract

Coleoid cephalopod molluscs comprise squid, cuttlefish and octopuses, and represent nearly the entire diversity of modern cephalopods. Sophisticated adaptations such as the use of colour for camouflage and communication, jet propulsion and the ink sac highlight the unique nature of the group. Despite these striking adaptations, there are clear parallels in ecology between coleoids and bony fishes. The coleoid fossil record is limited, however, hindering confident analysis of the tempo and pattern of their evolution. Here we use a molecular dataset (180 genes, approx. 36 000 amino acids) of 26 cephalopod species to explore the phylogeny and timing of cephalopod evolution. We show that crown cephalopods diverged in the Silurian–Devonian, while crown coleoids had origins in the latest Palaeozoic. While the deep-sea vampire squid and dumbo octopuses have ancient origins extending to the Early Mesozoic Era, 242 ± 38 Ma, incirrate octopuses and the decabrachian coleoids (10-armed squid) diversified in the Jurassic Period. These divergence estimates highlight the modern diversity of coleoid cephalopods emerging in the Mesozoic Marine Revolution, a period that also witnessed the radiation of most ray-finned fish groups in addition to several other marine vertebrates. This suggests that that the origin of modern cephalopod biodiversity was contingent on ecological competition with marine vertebrates.

Genus-level phylogeny of cephalopods using molecular markers: current status and problematic areas

“…This produced estimated divergence times of ∼220 Mya between the Octobrachia and Vampyromorphida, and 150 and 170 Mya for Decabrachia and Octobrachia lineages, respectively. This is roughly consistent with recent studies, including estimates based on the fossil record ( Kroger, Vinther & Fuchs, 2011 ), transcriptomic studies (∼212 and ∼219 Mya for Octobrachia and Decabrachia, respectively in Tanner et al, 2017 ), and other markers ( Warnke et al, 2011 ). Interestingly, the divergence between the major decabrachian lineages appears to have occurred within a relatively short period of time (e.g., within a 20 million-year time frame for the Loliginidae).…”

“…Additionally, several families that are believed to be closely related, for example Histioteuthidae-Psychroteuthidae, Lepidoteuthidae-Octopoteuthidae and Chiroteuthidae-Mastigoteuthidae-Batoteuthidae, were not recovered as monophyletic clades. These families show better support for a different phylogenetic position in previous studies ( Lindgren, 2010 , Lindgren et al, 2012 ; Tanner et al, 2017 ; Uribe & Zardoya, 2017 ).…”

“…Contrary to previous studies suggesting that Idiosepius diverged early (e.g., Sutton, Perales-Raya & Gilbert, 2016 ), in the present study, it forms a clade with the Loliginidae and Spirulidae in both the coleoid-inclusive and Decabrachia-only trees. This is also contrary to the monophyletic relationship of Idiosepius and Sepiolida that is strongly supported by mitochondrial gene rearrangements ( Strugnell et al, 2017 ) and transcriptomic data ( Tanner et al, 2017 ). Our results may thus be an artefact of the genes chosen for analysis since (similar to our study), Strugnell et al (2017) found Idiosepius to be an unsupported sister taxon to the Loliginidae when based on the mitochondrial genes alone.…”

Pattern of sucker development in cuttlefishes

“…1C, D). In Sepiida, which is thought to be an early-branched group among Decapodiformes (although there are several hypotheses about this [26,27]), the sucker morphology is relatively simple without specialized structures such as hooks [15] and is thought to show an ancestral state with some species diversity. Between the two focal cuttle sh species, few or no differences were observed in the sucker structures ( Fig.…”

Seagrass and cuttlefish—an historic association

“…Although sepiids may have had an origin in the Early Cretaceous (Kröger et al, 2011), the first fossil evidence is from the Late Cretaceous . A molecular age suggests a separation age of 88 Ma for sepiids (Tanner et al, 2017), just prior to the appearance of seagrass in the early Campanian (Late Cretaceous).…”