Brain size, life history, and metabolism at the marsupial/placental dichotomy

Abstract

The evolution of mammalian brain size is directly linked with the evolution of the brain's unique structure and performance. Both maternal life history investment traits and basal metabolic rate (BMR) correlate with relative brain size, but current hypotheses regarding the details of these relationships are based largely on placental mammals. Using encephalization quotients, partial correlation analyses, and bivariate regressions relating brain size to maternal investment times and BMR, we provide a direct quantitative comparison of brain size evolution in marsupials and placentals, whose reproduction and metabolism differ extensively. Our results show that the misconception that marsupials are systematically smaller-brained than placentals is driven by the inclusion of one large-brained placental clade, Primates. Marsupial and placental brain size partial correlations differ in that marsupials lack a partial correlation of BMR with brain size. This contradicts hypotheses stating that the maintenance of relatively larger brains requires higher BMRs. We suggest that a positive BMR-brain size correlation is a placental trait related to the intimate physiological contact between mother and offspring during gestation. Marsupials instead achieve brain sizes comparable to placentals through extended lactation. Comparison with avian brain evolution suggests that placental brain size should be constrained due to placentals' relative precociality, as has been hypothesized for precocial bird hatchlings. We propose that placentals circumvent this constraint because of their focus on gestation, as opposed to the marsupial emphasis on lactation. Marsupials represent a less constrained condition, demonstrating that hypotheses regarding placental brain size evolution cannot be generalized to all mammals.

Fig. 1.

Boxplots of EQ values in therian superorders. Error bars represent SD. Marsupials are not systematically smaller-brained than placentals, but Euarchontoglires is significantly larger-brained than most other therian superorders, due largely to the inclusion of Primates in this clade. The y axis is condensed between 4 and 7 to show the large EQ of Homo sapiens.

Fig. 2.

Regressions of (A) log brain size (in g; marsupials, n = 198; placentals, n = 493) with the marsupial Peramelemorpha shown separately; (B) log BMR (in KJ/h; marsupials, n = 68; placentals, n = 546); and (C) log maternal investment time (gestation + weaning in days; marsupials, n = 76; placentals, n = 91) against log body size (in g), with Peramelemorpha and the placental clade of Primates shown separately.

Fig. 3.

Flow diagrams of significant partial correlations of body size-adjusted gestation, weaning age, litter size, BMR, and brain weight. Empty arrows indicate negative correlations; numbers in italics indicate marginal significance (P = 0.05–0.1).

Fig. 4.

Schematic presentation of the relationships among maternal investment periods, neonatal maturity, and brain size proposed in this study. In placentals and precocial birds, neonatal/hatchling brain size is larger after a longer period of gestation or incubation. Brain growth of marsupials and altricial birds is achieved predominantly through extended lactation or posthatching care. Placentals have an extended period of placentation, which allows for more extensive prenatal brain growth compared with marsupials and precocial birds. The relative size of adult and neonatal/hatchling brain cartoons, and the relative durations, correspond to actual data for the species depicted (except for the neonatal brain of the gray kangaroo, which would have been too small to be visible). Hares and gray kangaroos have similar encephalizations. Data on brain sizes and durations are from various sources (17, 31, 72, 74).