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. 2017 Mar 15;284(1850):20162818.
doi: 10.1098/rspb.2016.2818.

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

Alastair R Tanner  1 , Dirk Fuchs  2 , Inger E Winkelmann  3 , M Thomas P Gilbert  3   4   5 , M Sabrina Pankey  6 , Ângela M Ribeiro  3 , Kevin M Kocot  7 , Kenneth M Halanych  8 , Todd H Oakley  9 , Rute R da Fonseca  3   10 , Davide Pisani  1   11 , Jakob Vinther  12   11
Affiliations

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

Alastair R Tanner et al. Proc Biol Sci. .

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.

Keywords: Cephalopoda; molecular clocks; molecular phylogenetics; phylogenomics.

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Figures

Figure 1.
Figure 1.
Molecular phylogeny of cephalopod, gastropod and bivalve molluscs (plus a scaphopod), with annelid outgroup; 180 genes, concatenated as 36 156 aligned amino acid positions with 26% missing data, modelled under CAT + GTR + Γ. Numbers at nodes denote Bayesian posterior probability/bootstrap support as returned by RAxML under the LG [33] substitution model. Scale bar is expected substitutions per site.
Figure 2.
Figure 2.
Phylogeny of 26 cephalopod species, plus outgroups (further details in figure 1); 180 genes, concatenated as 36 156 aligned amino acid positions with 26% missing data, modelled under CAT + GTR + Γ. Numbers at nodes denote Bayesian posterior probability/bootstrap support as returned by RAxML under the LG [33] substitution mode. Dotted branches at base of phylogeny are shortened for clarity, and outgroups (26 gastropods and bivalves, one scaphopod, four annelids) are collapsed for clarity (figure 1). Scale bar is expected substitutions per site.
Figure 3.
Figure 3.
Comparison of molecular clock model and calibration scheme on confidence intervals for node timing inference. (a) Applying CIR clock model, (b) applying uncorrelated gamma multipier model. Red bars at nodes are confidence intervals with only calibrations external to cephalopods applied. Blue bars are confidence intervals with the full calibration applied. Grey bars are the joint prior distribution at nodes. Not all nodes are labelled to aid clarity, full details in the electronic supplementary material.
Figure 4.
Figure 4.
Chronogram of cephalopods, plus 26 bivalve and gastropod molluscs, one scaphopod and four annelids as outgroups and calibration nodes; 36 156 amino acid positions analysed under CAT-GTR substitution model, CIR clock model, Yule birth–death process, soft bound of 0.05, and a root prior of 565 Ma with a standard deviation of ±10 Ma. Bars at nodes represent 95% confidence intervals (recent nodes not labelled with bars to aid clarity). Red dots indicated calibrated nodes (electronic supplementary material, table S1 and figure S3); red dotted lines represent extent of calibration minima. Environmental conditions and sea-level curve simplified from Miller et al. [45]. Curves for belemnite, actinopterygian, chondrichthyan and Palaeozoic fish diversity are based on fossil observations on diversity, data from Palaeobiology Database (pbdb.org), electronic supplementary material, table S5. Red vertical lines represent major extinction events. Aqua-blue vertical bar signifies the extent of the Mesozoic Marine Revolution [10].
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