Coleoid Cephalopods Demonstrate Asocial Path to the Evolution of Big Brains

Abstract

Social factors have been argued to be the main selection pressure for the evolution of large brains and complex behavior on the basis of data from mammals and birds. Coleoid cephalopods (octopuses, squid, and cuttlefish) have large brains, complex nervous systems and show signs of intelligent behavior comparable to that of primates, cetaceans, and birds. However, many cephalopods live largely solitary, semelparous, short lives, and many are cannibalistic, leaving little to no opportunity for parental care, complex group dynamics, or social learning. This suggests that the large brains found in cephalopods are not the result of social selection pressures. Here, motivated by the predictions of the "Asocial Brain Hypothesis", a yet untested regime of the Cultural Brain Hypothesis formal model, we compare the relationships between brain size and social, ecological, and other factors in cephalopods. Consistent with the prediction that ecological factors should be the primary selection pressure with larger brains in more calorie-rich complex ecologies, we find that shallower and benthic (seafloor) habitats--arguably more complex environments than open-ocean (pelagic) habitats--are associated with larger brain sizes, and that measures of sociality are not. Our findings from these highly divergent evolutionary lineages, which diverged from vertebrates over 500 million years ago are not causal, but are consistent with the "Asocial Brain Hypothesis" mechanistic model that describes how ecological selection pressures can also produce large, complex brains.