Being fat and smart: A comparative analysis of the fat-brain trade-off in mammals

Abstract

Humans stand out among non-aquatic mammals by having both an extremely large brain and a relatively large amount of body fat. To understand the evolution of this human peculiarity we report a phylogenetic comparative study of 120 mammalian species, including 30 primates, using seasonal variation in adult body mass as a proxy of the tendency to store fat. Species that rely on storing fat to survive lean periods are expected to be less active because of higher costs of locomotion and have increased predation risk due to reduced agility. Because a fat-storage strategy reduces the net cognitive benefit of a large brain without reducing its cost, such species should be less likely to evolve a larger brain than non-fat-storing species. We therefore predict that the two strategies to buffer food shortages (storing body fat and cognitive flexibility) are compensatory, and therefore predict negative co-evolution between relative brain size and seasonal variation in body mass. This trade-off is expected to be stronger in predominantly arboreal species than in more terrestrial ones, as the cost of transporting additional adipose depots is higher for climbing than for horizontal locomotion. We did, indeed, find a significant negative correlation between brain size and coefficient of variation (CV) in body mass in both sexes for the subsample of arboreal species, both in all mammals and within primates. In predominantly terrestrial species, in contrast, this correlation was not significant. We therefore suggest that the adoption of habitually terrestrial locomotor habits, accompanied by a reduced reliance on climbing, has allowed for a primate of our body size the unique human combination of unusually large brains and unusually large adipose depots.

The effect of body size evolution and ecology on encephalization in cave bears and extant relatives

“…Bear species, which do not exhibit dormancy and have a high caloric diet, showed a weak but significant correlation with bigger relative brain size. This would be in accordance with the trait-off between brain size and adipose tissue as well as studies on diet and brain size [60, 66–68]. The ecological shift towards a plant based diet alone did not affect encephalization in cave bears.…”

“…Dormancy and diet, separately, were not correlated with brain size; however, the combination of both variables showed a significant effect. A possible explanation for this correlation could be that cave bears underwent a change in diet in a habitat in which they were still forced to rest during winters [1, 9] limiting the possibility of so called cognitive buffering [66, 109]. Under the Cognitive Buffer hypothesis, it is expected that relative brain size of mammals in highly seasonal environment increases due to the necessity of behavioural flexibility.…”

“…This, however, also implies an active reaction towards the environmental change. In contrast, dormancy does not require this high level of behavioural flexibility but relies on body fat storage, which additionally has a negative trade-off with brain size [60, 66]. This suggests that brain size in cave bears might exhibit a physiological buffering effect [66] partly constraining relative brain size.…”

“…In contrast, dormancy does not require this high level of behavioural flexibility but relies on body fat storage, which additionally has a negative trade-off with brain size [60, 66]. This suggests that brain size in cave bears might exhibit a physiological buffering effect [66] partly constraining relative brain size. Other bear species such as U. arctos and U. americanus would also exhibit this physiological buffering effect but their food quality or life history might lessen the constraint on relative brain size.…”

“…Brain tissue itself is known to be expensive to produce and maintain [43–45]. Absolute as well as relative brain size can be influenced by social structure [46–48], environment [48–52], sensory systems [53], evolutionary history [54–57], body size evolution [42], and different physiological as well as life history trade-offs [43, 52, 57–66]. …”