Grow Smart and Die Young: Why Did Cephalopods Evolve Intelligence?
Authors: Piero Amodio, Markus Boeckle, Alexandra K. Schnell, Ljerka Ostojíc, Graziano Fiorito, Nicola S. Clayton
Journal: Trends in Ecology & Evolution (2018)

The most influential views on the evolution of intelligence suggest that intelligence coevolves with slow life history in response to socioecological challenges; however, these conclusions are primarily focused on large-brained vertebrates. Cephalopod molluscs strongly challenge the most accepted hypotheses on the evolution of intelligence: cephalopods evolved complex brains and high behavioural flexibility together with fast life histories and in simple social environments. Surprisingly, the evolution of intelligence in cephalopods has been largely overlooked, thus leaving this evolutionary conundrum unsolved. Discussing differences and similarities between cephalopods and large-brained vertebrates, may shed light on fundamental aspects of the evolution of intelligence. Intelligence in large-brained vertebrates might have evolved through independent, yet similar processes based on comparable socioecological pressures and slow life histories. This convergent evolutionary route, however, cannot explain why cephalopods developed large brains and flexible behavioural repertoires: cephalopods have fast life histories and live in simple social environments. Here, we suggest that the loss of the external shell in cephalopods (i) caused a dramatic increase in predatory pressure, which in turn prevented the emergence of slow life histories, and (ii) allowed the exploitation of novel challenging niches, thus favouring the emergence of intelligence. By highlighting convergent and divergent aspects between cephalopods and large-brained vertebrates we illustrate how the evolution of intelligence might not be constrained to a single evolutionary route. Intelligence in large-brained vertebrates might have evolved through independent, yet similar processes based on comparable socioecological pressures and slow life histories. This convergent evolutionary route, however, cannot explain why cephalopods developed large brains and flexible behavioural repertoires: cephalopods have fast life histories and live in simple social environments. Here, we suggest that the loss of the external shell in cephalopods (i) caused a dramatic increase in predatory pressure, which in turn prevented the emergence of slow life histories, and (ii) allowed the exploitation of novel challenging niches, thus favouring the emergence of intelligence. By highlighting convergent and divergent aspects between cephalopods and large-brained vertebrates we illustrate how the evolution of intelligence might not be constrained to a single evolutionary route. Cognitive complexity varies dramatically across species, from simple reflexes to sophisticated intelligence (see Glossary) supporting high behavioural flexibility. Traditionally, primates have been considered the pinnacle of cognitive complexity, thus representing the primary target for investigating the evolution of intelligence. Evidence collected in monkeys and apes led to specific hypotheses about the conditions favouring the emergence of intelligence. Firstly, primate intelligence has thought to have evolved as an adaptation to cope with particularly challenging socioecological niches (Box 1). Two key factors are considered to have driven this adaptation: the need to find and process food (Ecological Intelligence Hypothesis [1Byrne R.W. The technical intelligence hypothesis: an additional evolutionary stimulus to intelligence.in: Whiten A. Byrne R. Machiavellian Intelligence II. Cambridge University Press, 1997: 289-311Crossref Google Scholar, 2Janmaat K.R.L. et al.Spatio-temporal complexity of chimpanzee food: How cognitive adaptations can counteract the ephemeral nature of ripe fruit.Am. J. Primatol. 2016; 78: 626-645Crossref PubMed Scopus (7) Google Scholar, 3Gibson K.R. Cognition, brain size and the extraction of embedded food resources.Primate Ontogeny, Cognition and Social Behaviour. Cambridge University Press, 1986: 93-103Google Scholar]), and the demands of complex social bonds (Social Intelligence Hypothesis [4van Schaik C.P. Burkart J.M. Social learning and evolution: the cultural intelligence hypothesis.Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2011; 366: 1008-1016Crossref PubMed Scopus (0) Google Scholar, 5Byrne R.W. Whiten A. Machiavellian Intelligence: Social Expertise and the Evolution of Intellect in Monkeys, Apes, and Humans. Clarendon Press, 1988Google Scholar, 6Dunbar R.I.M. The Social Brain Hypothesis.Evol. Anthropol. 1998; 9: 178-190Crossref Scopus (1142) Google Scholar]). Second, the positive correlation between brain size and the long developmental trajectory reported in primates [7Street S.E. et al.Coevolution of cultural intelligence, extended life history, sociality, and brain size in primates.Proc. Natl. Acad. Sci. U. S. A. 2017; 114: 7908-7914Crossref PubMed Scopus (14) Google Scholar] suggests a coevolutionary scenario for the evolution of these traits. The slow life history might have been necessary to overcome the costs of a large brain and/or a consequence of the reduced extrinsic mortality resulting from enhanced intelligence [8Sol D. Revisiting the cognitive buffer hypothesis for the evolution of large brains.Biol. Lett. 2009; 5: 130-133Crossref PubMed Scopus (0) Google Scholar, 9Barton R.A. Capellini I. Maternal investment, life histories, and the costs of brain growth in mammals.Proc. Natl. Acad. Sci. U. S. A. 2011; 108: 6169-6174Crossref PubMed Scopus (0) Google Scholar].Box 1Main Hypotheses for the Evolution of IntelligenceThe most accepted hypotheses for the evolution of complex cognition can be divided into two categories. The Ecological Intelligence Hypothesis suggests that complex cognition evolved to meet the challenges associated with finding and processing food [1Byrne R.W. The technical intelligence hypothesis: an additional evolutionary stimulus to intelligence.in: Whiten A. Byrne R. Machiavellian Intelligence II. Cambridge University Press, 1997: 289-311Crossref Google Scholar, 2Janmaat K.R.L. et al.Spatio-temporal complexity of chimpanzee food: How cognitive adaptations can counteract the ephemeral nature of ripe fruit.Am. J. Primatol. 2016; 78: 626-645Crossref PubMed Scopus (7) Google Scholar, 3Gibson K.R. Cognition, brain size and the extraction of embedded food resources.Primate Ontogeny, Cognition and Social Behaviour. Cambridge University Press, 1986: 93-103Google Scholar]. Specifically, features such as spatiotemporally dispersed food, generalist diets, and extractive foraging are considered key drivers in this process. Conversely, the Social Intelligence Hypothesis accredits the evolution of intelligence to the demands of group living, such as maintaining complex and enduring social bonds, deception, cooperation, or social learning from conspecifics [4van Schaik C.P. Burkart J.M. Social learning and evolution: the cultural intelligence hypothesis.Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2011; 366: 1008-1016Crossref PubMed Scopus (0) Google Scholar, 5Byrne R.W. Whiten A. Machiavellian Intelligence: Social Expertise and the Evolution of Intellect in Monkeys, Apes, and Humans. Clarendon Press, 1988Google Scholar, 6Dunbar R.I.M. The Social Brain Hypothesis.Evol. Anthropol. 1998; 9: 178-190Crossref Scopus (1142) Google Scholar]. To date, support for both the Ecological Intelligence Hypothesis [96DeCasien A.R. et al.Primate brain size is predicted by diet but not sociality.Nat. Ecol. Evol. 2017; 1 (0112)Crossref PubMed Scopus (35) Google Scholar, 97Farris S.M. Schulmeister S. Parasitoidism, not sociality, is associated with the evolution of elaborate mushroom bodies in the brains of hymenopteran insects.Proceedings. Biol. Sci. 2011; 278: 940-951Crossref PubMed Scopus (0) Google Scholar, 98O'Donnell S. et al.Distributed cognition and social brains: reductions in mushroom body investment accompanied the origins of sociality in wasps (Hymenoptera: Vespidae).Proceedings. Biol. Sci. 2015; 282: 20150791Crossref PubMed Scopus (23) Google Scholar, 99Sayol F. et al.Environmental variation and the evolution of large brains in birds.Nat. Commun. 2016; 7: 13971Crossref PubMed Scopus (15) Google Scholar] and the Social Intelligence Hypothesis [100Pollen A.A. et al.Environmental complexity and social organization sculpt the brain in Lake Tanganyikan cichlid fish.Brain. Behav. Evol. 2007; 70: 21-39Crossref PubMed Scopus (0) Google Scholar, 101Ashton B.J. et al.Cognitive performance is linked to group size and affects fitness in Australian magpies.Nature. 2018; 554: 364-367Crossref PubMed Scopus (13) Google Scholar] has been demonstrated in different groups, mainly among mammals and birds. It must be noted however that these hypotheses are not mutually exclusive per se and that more recent approaches have worked towards frameworks accounting for both ecological and social pressures [68Dunbar R.I.M. Shultz S. Why are there so many explanations for primate brain evolution?.Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2017; 372 (20160244)Crossref PubMed Scopus (4) Google Scholar, 102Navarrete A.F. et al.The coevolution of innovation and technical intelligence in primates.Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2016; 371 (20150186)Crossref PubMed Scopus (20) Google Scholar].It has also been proposed that intelligence might have arisen as a cognitive adaptation to cope with the challenges of predator–prey interactions [86Byrne R.W. Bates L.A. Sociality, evolution and cognition.Curr. Biol. 2007; 17: R714-R723Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar, 103Zuberbühler K. Jenny D. Leopard predation and primate evolution.J. Hum. Evol. 2002; 43: 873-886Crossref PubMed Scopus (0) Google Scholar, 104Skelhorn J. Rowe C. Cognition and the evolution of camouflage.Proceedings. Biol. Sci. 2016; 283: 20152890Crossref PubMed Google Scholar, 105van der Bijl W. Kolm N. Why direct effects of predation complicate the social brain hypothesis.BioEssays. 2016; 38: 568-577Crossref PubMed Scopus (8) Google Scholar]. Capturing prey and avoiding predation have dramatic fitness consequences. Thus, it is not hard to imagine how complex cognition allowing flexible behaviours in these domains could be subject to strong positive selection. According to some authors, the cognitive challenges of predator–prey dynamics can be equivalent to those required to compete with group members as in both cases they require interactions with another individual pursuing personal gains [86Byrne R.W. Bates L.A. Sociality, evolution and cognition.Curr. Biol. 2007; 17: R714-R723Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar]. This hypothesis has been discussed for primates [103Zuberbühler K. Jenny D. Leopard predation and primate evolution.J. Hum. Evol. 2002; 43: 873-886Crossref PubMed Scopus (0) Google Scholar] and supported from investigations in distinct groups such as fish [106van der Bijl W. et al.Brain size affects the behavioural response to predators in female guppies (Poecilia reticulata).Proceedings. Biol. Sci. 2015; 282 (20151132)Crossref PubMed Google Scholar, 107Kotrschal A. et al.Predation pressure shapes brain anatomy in the wild.Evol. Ecol. 2017; 31: 619-633Crossref Scopus (9) Google Scholar], carnivores, and herbivores [108Jerison H.J. Evolution of the Brain and Intelligence. Academic Press, 1973Google Scholar, 109Köhler M. Moyà-Solà S. Reduction of brain and sense organs in the fossil insular bovid Myotragus.Brain. Behav. Evol. 2004; 63: 125-140Crossref PubMed Scopus (0) Google Scholar]. The most accepted hypotheses for the evolution of complex cognition can be divided into two categories. The Ecological Intelligence Hypothesis suggests that complex cognition evolved to meet the challenges associated with finding and processing food [1Byrne R.W. The technical intelligence hypothesis: an additional evolutionary stimulus to intelligence.in: Whiten A. Byrne R. Machiavellian Intelligence II. Cambridge University Press, 1997: 289-311Crossref Google Scholar, 2Janmaat K.R.L. et al.Spatio-temporal complexity of chimpanzee food: How cognitive adaptations can counteract the ephemeral nature of ripe fruit.Am. J. Primatol. 2016; 78: 626-645Crossref PubMed Scopus (7) Google Scholar, 3Gibson K.R. Cognition, brain size and the extraction of embedded food resources.Primate Ontogeny, Cognition and Social Behaviour. Cambridge University Press, 1986: 93-103Google Scholar]. Specifically, features such as spatiotemporally dispersed food, generalist diets, and extractive foraging are considered key drivers in this process. Conversely, the Social Intelligence Hypothesis accredits the evolution of intelligence to the demands of group living, such as maintaining complex and enduring social bonds, deception, cooperation, or social learning from conspecifics [4van Schaik C.P. Burkart J.M. Social learning and evolution: the cultural intelligence hypothesis.Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2011; 366: 1008-1016Crossref PubMed Scopus (0) Google Scholar, 5Byrne R.W. Whiten A. Machiavellian Intelligence: Social Expertise and the Evolution of Intellect in Monkeys, Apes, and Humans. Clarendon Press, 1988Google Scholar, 6Dunbar R.I.M. The Social Brain Hypothesis.Evol. Anthropol. 1998; 9: 178-190Crossref Scopus (1142) Google Scholar]. To date, support for both the Ecological Intelligence Hypothesis [96DeCasien A.R. et al.Primate brain size is predicted by diet but not sociality.Nat. Ecol. Evol. 2017; 1 (0112)Crossref PubMed Scopus (35) Google Scholar, 97Farris S.M. Schulmeister S. Parasitoidism, not sociality, is associated with the evolution of elaborate mushroom bodies in the brains of hymenopteran insects.Proceedings. Biol. Sci. 2011; 278: 940-951Crossref PubMed Scopus (0) Google Scholar, 98O'Donnell S. et al.Distributed cognition and social brains: reductions in mushroom body investment accompanied the origins of sociality in wasps (Hymenoptera: Vespidae).Proceedings. Biol. Sci. 2015; 282: 20150791Crossref PubMed Scopus (23) Google Scholar, 99Sayol F. et al.Environmental variation and the evolution of large brains in birds.Nat. Commun. 2016; 7: 13971Crossref PubMed Scopus (15) Google Scholar] and the Social Intelligence Hypothesis [100Pollen A.A. et al.Environmental complexity and social organization sculpt the brain in Lake Tanganyikan cichlid fish.Brain. Behav. Evol. 2007; 70: 21-39Crossref PubMed Scopus (0) Google Scholar, 101Ashton B.J. et al.Cognitive performance is linked to group size and affects fitness in Australian magpies.Nature. 2018; 554: 364-367Crossref PubMed Scopus (13) Google Scholar] has been demonstrated in different groups, mainly among mammals and birds. It must be noted however that these hypotheses are not mutually exclusive per se and that more recent approaches have worked towards frameworks accounting for both ecological and social pressures [68Dunbar R.I.M. Shultz S. Why are there so many explanations for primate brain evolution?.Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2017; 372 (20160244)Crossref PubMed Scopus (4) Google Scholar, 102Navarrete A.F. et al.The coevolution of innovation and technical intelligence in primates.Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2016; 371 (20150186)Crossref PubMed Scopus (20) Google Scholar]. It has also been proposed that intelligence might have arisen as a cognitive adaptation to cope with the challenges of predator–prey interactions [86Byrne R.W. Bates L.A. Sociality, evolution and cognition.Curr. Biol. 2007; 17: R714-R723Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar, 103Zuberbühler K. Jenny D. Leopard predation and primate evolution.J. Hum. Evol. 2002; 43: 873-886Crossref PubMed Scopus (0) Google Scholar, 104Skelhorn J. Rowe C. Cognition and the evolution of camouflage.Proceedings. Biol. Sci. 2016; 283: 20152890Crossref PubMed Google Scholar, 105van der Bijl W. Kolm N. Why direct effects of predation complicate the social brain hypothesis.BioEssays. 2016; 38: 568-577Crossref PubMed Scopus (8) Google Scholar]. Capturing prey and avoiding predation have dramatic fitness consequences. Thus, it is not hard to imagine how complex cognition allowing flexible behaviours in these domains could be subject to strong positive selection. According to some authors, the cognitive challenges of predator–prey dynamics can be equivalent to those required to compete with group members as in both cases they require interactions with another individual pursuing personal gains [86Byrne R.W. Bates L.A. Sociality, evolution and cognition.Curr. Biol. 2007; 17: R714-R723Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar]. This hypothesis has been discussed for primates [103Zuberbühler K. Jenny D. Leopard predation and primate evolution.J. Hum. Evol. 2002; 43: 873-886Crossref PubMed Scopus (0) Google Scholar] and supported from investigations in distinct groups such as fish [106van der Bijl W. et al.Brain size affects the behavioural response to predators in female guppies (Poecilia reticulata).Proceedings. Biol. Sci. 2015; 282 (20151132)Crossref PubMed Google Scholar, 107Kotrschal A. et al.Predation pressure shapes brain anatomy in the wild.Evol. Ecol. 2017; 31: 619-633Crossref Scopus (9) Google Scholar], carnivores, and herbivores [108Jerison H.J. Evolution of the Brain and Intelligence. Academic Press, 1973Google Scholar, 109Köhler M. Moyà-Solà S. Reduction of brain and sense organs in the fossil insular bovid Myotragus.Brain. Behav. Evol. 2004; 63: 125-140Crossref PubMed Scopus (0) Google Scholar]. More recently, indicators of complex cognition have been reported in distantly related lineages, most notably cetaceans, elephants, corvids, and parrots [10Fox K.C.R. et al.The social and cultural roots of whale and dolphin brains.Nat. Ecol. Evol. 2017; 1: 1699-1705Crossref PubMed Scopus (6) Google Scholar, 11Emery N.J. Clayton N.S. The mentality of crows: convergent evolution of intelligence in corvids and apes.Science. 2004; 306: 1903-1907Crossref PubMed Scopus (572) Google Scholar, 12Plotnik J.M. Clayton N.S. Convergent cognitive evolution across animal taxa: comparisons of chimpanzees, corvids, and elephants.The Conceptual Mind: New Directions in the Study of Concepts. MIT Press, 2015: 29-55Google Scholar]. This discovery allows us to investigate the evolution of intelligence beyond primates and thus deepen our understanding of this process. Differences in evolutionary history and brain structure between apes and these taxa suggest that (i) intelligence emerged multiple times independently [13Roth G. Convergent evolution of complex brains and high intelligence.Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2015; 370 (20150049)Crossref PubMed Scopus (14) Google Scholar]; and (ii) distinct neural substrates such as the avian nidopallium and the mammalian cortex, can support equivalent cognitive sophistication [14Güntürkün O. Bugnyar T. Cognition without Cortex.Trends Cogn. Sci. 2016; 20: 291-303Abstract Full Text Full Text PDF PubMed Scopus (45) Google Scholar]. Despite these differences, the socioecological challenges faced by cetaceans, elephants, corvids, and parrots appear to be comparable to those of apes. Thus, intelligence might have evolved convergently in these groups in response to similar selective pressures [10Fox K.C.R. et al.The social and cultural roots of whale and dolphin brains.Nat. Ecol. Evol. 2017; 1: 1699-1705Crossref PubMed Scopus (6) Google Scholar, 11Emery N.J. Clayton N.S. The mentality of crows: convergent evolution of intelligence in corvids and apes.Science. 2004; 306: 1903-1907Crossref PubMed Scopus (572) Google Scholar, 12Plotnik J.M. Clayton N.S. Convergent cognitive evolution across animal taxa: comparisons of chimpanzees, corvids, and elephants.The Conceptual Mind: New Directions in the Study of Concepts. MIT Press, 2015: 29-55Google Scholar]. Furthermore, as with primates, a tight link between brain size and slow life history also exists in birds and other mammals [15Gonzales-Lagos C. et al.Large-brained mammals live longer.J. Evol. Biol. 2010; 23: 1064-1074Crossref PubMed Scopus (40) Google Scholar, 16Minias P. Podlaszczuk P. Longevity is associated with relative brain size in birds.Ecol. Evol. 2017; 7: 3558-3566Crossref PubMed Scopus (1) Google Scholar]. Therefore, similar evolutionary trade-offs might have acted during the evolution of intelligence in distantly related groups of vertebrates. This convergent evolutionary route, however, cannot explain why intelligence evolved in cephalopods (Figure 1). Coleoid cephalopods (cuttlefish, squid, and octopuses) are shell-less molluscs that are considered among the most cognitively advanced group of invertebrates. They evolved a unique mixture of convergent and divergent features relative to the main groups of intelligent vertebrates (Table 1). On the one hand, cephalopods are endowed with a sophisticated nervous system, which both resembles that of vertebrates in relative size [17Packard A. Cephalopods and fish: the limits of convergence.Biol. Rev. 1972; 47: 241-307Crossref Google Scholar] and complexity [18Hochner B. et al.The octopus: a model for a comparative analysis of the evolution of learning and memory mechanisms.Biol. Bull. 2006; 210: 308-317Crossref PubMed Scopus (0) Google Scholar, 19Young J.Z. Computation in the learning system of cephalopods.Biol. Bull. 1991; 180: 200-208Crossref PubMed Google Scholar] and supports strikingly flexible behavioural repertoires [20Mather J.A. Dickel L. Cephalopod complex cognition.Curr. Opin. Behav. Sci. 2017; 16: 131-137Crossref Scopus (5) Google Scholar, 21Darmaillacq A.-S. et al.Cephalopod Cognition. Cambridge University Press, 2014Crossref Scopus (18) Google Scholar, 22Marini G. et al.Behavioral Analysis of Learning and Memory in Cephalopods.in: Byrne J.H. 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Soc. 2001; 76 (S1464793101005681)Crossref PubMed Scopus (196) Google Scholar].Table 1Convergent and Divergent Features between Cephalopods and Large-Brained VertebratesaThe colours of the cells refer to traits that are variable across the groups (blue), or shared (green) or not shared (orange) between the cephalopods and groups of vertebrates.TraitCephalopodsCorvidsCetaceansApesMorphologyManipulative appendagesSuckered arms and tentaclesBeak and feetRostrumHandsDexterityHighHighLimitedHighSensesVisionHighHighHighHighAcousticLimitedHighHighHighSmellchemotacticHighLimitedLimitedLimitedBrainBrain–body size ratioHighHighHighHighSubstrate for complex cognitionVertical lobeNidopalliumCortexCortexEcologyLifestyleAquaticFlightAquaticTerrestrial/arborealDietCarnivoresGeneralisticCarnivoresGeneralisticExtractive foragingPresentPresentAbsentPresentPredationHighLimitedLimitedLimitedSocial LifeSystemSolitary/anonymous schoolsPairs/groupsFamily groupsGroupsLong-term bondsAbsentWith pair mateWith multiple individualsWith multiple individualsBehavioural flexibilityFind and process foodHighHighHighHighSocial interactionsLimited?HighHighHighPredator avoidanceHigh???Life HistoryLifespan0.5–2 years>15 years>40 years>40 yearsParental care of offspringAbsentPresentPresentPresentReproductionSemelparousstrategiesIteroparityIteroparityIteroparitya The colours of the cells refer to traits that are variable across the groups (blue), or shared (green) or not shared (orange) between the cephalopods and groups of vertebrates. Open table in a new tab Here, we present the current reports of behavioural convergence in cephalopods and cognitively advanced vertebrates. We also discuss the factors leading to the emergence of intelligence and fast life histories in cephalopods, highlighting the convergent and divergent aspects between cephalopods and large-brained vertebrates. We contend that vital insights into the evolution of intelligence can be gained by investigating cephalopod cognition. Intelligence cannot be measured directly, thus, it is typically estimated through morphological and behavioural proxies; namely brain features, and behavioural flexibility. Although different in many aspects, cephalopod brains resemble those of vertebrates in relative size and complexity (Box 2). However, because the cognitive underpinnings of behavioural flexibility have rarely been investigated in this group (although, see [26Yang T.-I. Chiao C.-C. Number sense and state-dependent valuation in cuttlefish.Proceedings. Biol. Sci. 2016; 283 (20161379)Crossref Scopus (6) Google Scholar, 27Jozet-Alves C. et al.Evidence of episodic-like memory in cuttlefish.Curr. Biol. 2013; 23: R1033-R1035Abstract Full Text Full Text PDF PubMed Google Scholar]), current evidence does not allow a fine-grained assessment of intelligence in cephalopods. Flexible behaviours can be supported by simple cognitive mechanisms [28Mikhalevich I. et al.Is behavioural flexibility evidence of cognitive complexity? How evolution can inform comparative cognition.Interface Focus. 2017; 7 (20160121)Crossref PubMed Scopus (4) Google Scholar, 29Shettleworth S.J. Cognition, Evolution, and Behavior. Oxford University Press, 2010Google Scholar, 30Seed A. et al.Intelligence in corvids and apes: a case of convergent evolution?.Ethology. 2009; 115: 401-420Crossref Scopus (0) Google Scholar], thus, the interpretation of behavioural evidence for intelligence in cephalopods requires caution. Nevertheless, the behavioural convergence between cephalopods and intelligent vertebrates appears remarkable. Below, we highlight the most striking evidence of behavioural flexibility and why these behaviours might require complex cognitive mechanisms.Box 2Nervous System of CephalopodsCephalopods have a remarkably large nervous system (up to 500 million neuronal cells in the octopus) that comprises a unique mixture of classic molluscan features and more complex vertebrate-like traits [110Shigeno S. et al.Cephalopod brains: an overview of current knowledge to facilitate comparison with vertebrates.Front. Physiol. 2018; 9: 952Crossref PubMed Scopus (0) Google Scholar]. The brain is formed by the aggregation of several ganglia (i.e., lobes) that show the typical neuronal arrangement of invertebrates, with cell bodies surrounding internal layers of synaptic connections [111Young J.Z. The Anatomy of the Nervous System of Octopus vulgaris. Clarendon Press, 1971Google Scholar]. However, the relative size of the cephalopod brain (corrected for body size) [17Packard A. Cephalopods and fish: the limits of convergence.Biol. Rev. 1972; 47: 241-307Crossref Google Scholar] and the high density of interneurons resemble that of some vertebrates [19Young J.Z. Computation in the learning system of cephalopods.Biol. Bull. 1991; 180: 200-208Crossref PubMed Google Scholar, 112Shomrat T. et al.The vertical lobe of cephalopods: an attractive brain structure for understanding the evolution of advanced learning and memory systems.J. Comp. Physiol. A. 2015; 201: 947-956Crossref PubMed Google Scholar, 113Young J.Z. et al.Multiple matrices in the memory system of Octopus.in: Abbott N.J. Cephalopod Neurobiology : Neuroscience Studies in Squid, Octopus, and Cuttlefish. Oxford University Press, 1995: 431-443Crossref Google Scholar].The number and function of the lobes differ substantially across cephalopods, depending on species-specific lifestyles [114Nixon M. Young J.Z. The Brains and Lives of Cephalopods. Oxford University Press, 2003Google Scholar]. Among the various lobes that constitute the cephalopod brain, the vertical lobe plays a pivotal role in learning and memory in all coleoids [60Grasso F.W. Basil J.A. The evolution of flexible behavioral repertoires in cephalopod molluscs.Brain. Behav. Evol. 2009; 74: 231-245Crossref PubMed Scopus (51) Google Scholar, 115Fiorito G. Chichery R. Lesions of the vertical lobe impair visual discrimination learning by observation in Octopus vulgaris.Neurosci. Lett. 1995; 192: 117-120Crossref PubMed Google Scholar], and has been compared to regions of the mammalian cortex and avian nidopallium [113Young J.Z. et al.Multiple matrices in the memory system of Octopus.in: Abbott N.J. Cephalopod Neurobiology : Neuroscience Studies in Squid, Octopus, and Cuttlefish. Oxford University Press, 1995: 431-443Crossref Google Scholar, 116Edelman D.B. Seth A.K. Animal consciousness: a synthetic approach.Trends Neurosci. 2009; 32: 476-484Abstract Full Text Full Text PDF PubMed Scopus (68) Google Scholar]. In contrast to birds and mammals, the processing of motor and sensory inputs in cephalopods is only partially dependent on the central brain. The optic lobes, a pair of large nervous structures located outside the cartilaginous capsule of the brain and connected to the retinae of the lens eyes, are essential for the computation of visual input [113Young J.Z. et al.Multiple matrices in the memory system of Octopus.in: Abbott N.J. Cephalopod Neurobiology : Neuroscience Studies in Squid, Octopus, and Cuttlefish. Oxford University Press, 1995: 431-443Crossref Google Scholar]. Furthermore, the processing of chemotactile information and of the motor programmes is performed through the concerted action of higher centres (i.e., the inferior frontal lobe system, [