Macroevolution of Toothed Whales Exceptional Relative Brain Size

Toothed whales (Odontoceti, Cetacea) are well-known for their ability to produce complex vocalizations, to use tools, to possess self-recognition, and for their extreme behavioural plasticity. The toothed whale intelligence is said to compete with that of primates, so does their extremely large brain to body size ratio. Common explanations for the acquisition of such large brains over the evolutionary time (encephalization) in toothed whales range from their demanding, complex social lives, to their feeding habits, to echolocation. Yet, several studies found no macroevolutionary trend in Odontoceti encephalization, which casts doubts on its selective advantage. We applied a recently developed phylogenetic comparative method to study macroevolutionary trends in relative brain size (RBS) and brain size evolutionary rates in cetaceans, comparing toothed whales to the other cetaceans and contrasting groups of species as ascribed to different feeding categories. We found that cetaceans as a whole followed a trend for increased encephalization over time, starting from small-brained archaeocete ancestors. Toothed whales do not show this same trend in RBS but have possessed larger RBS than any other cetacean ever since the beginning of their existence. The rate of RBS evolution in Odontoceti is significantly slower than in other Cetacea and slower than the rate of Odontoceti body size evolution. These results suggest that toothed whales’ history is characterized by high and conservative relative encephalization. Feeding lifestyle does not explain these patterns, while the appearance of echolocation within stem group Odontoceti remains a viable candidate for them.