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 BMRbrain 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.encephalization | maternal energy hypothesis | altricial | basal metabolic rate M ammalian brain size is widely relevant to neuroscience. Aside from the classical interpretation of brain size as a proxy for cognitive or sensorimotor capacity (1-3), brain size corresponds to the macroscopic, microstructural, and connective composition of the mammalian brain with remarkable accuracy (4, 5). However, despite decades of research, the factors underlying the evolution of brain size relative to body size (referred to as "brain size" hereafter), particularly relative brain enlargement, remain a matter of debate (6). Maternal life history investment traits, such as gestation and litter size, are generally accepted as mammalian brain size correlates (7-13) and are considered to reflect a female's ability to energetically provision her offspring's brain growth (14,(15)(16)(17). A more controversial potential brain size correlate is basal metabolic rate (BMR) (18,19). Recent studies have confirmed a consistent correlation between increased brain size and BMR across placentals (20, 21), although this does not apply to all placental clades (8,22).Interpretations as to why BMR should influence mammalian brain size vary. It has been suggested t...

Maternal investment, life histories, and the costs of brain growth in mammals

“…This idea overlaps with the "maternal energy hypothesis," which suggests that maternal investment and energy availability constrain the development of large brains, predicting that brain size correlates with the duration of maternal investment and with maternal basal metabolic rate (BMR) (11,12). Recent comparative evidence is consistent with both cognitive buffer and developmental cost ideas; brain size variation in adult mammals is positively correlated with lifespan (6, 7) as well as with the durations of gestation, lactation, and the juvenile period (4,5,8,13,14).…”

“…Many comparative studies have been aimed at understanding how and why such variation evolved, and have identified a range of factors associated with the evolution of large brains. One general factor robustly correlated with brain size is life history; larger-brained species, such as humans, develop slowly and have extended periods of juvenility and long lifespans, effects that remain after accounting for differences in body size (1)(2)(3)(4)(5)(6)(7)(8). These associations have been interpreted in two different ways.…”

“…The cognitive buffer hypothesis predicts correlations among brain size, survival, and lifespan (6,7). Developmental costs hypotheses, on the other hand, assume that brain growth is traded off against aspects of production, including growth, maturation time, and reproductive rates, causing largerbrained species to grow and mature more slowly and to have lower fertility (4,5,(8)(9)(10). This idea overlaps with the "maternal energy hypothesis," which suggests that maternal investment and energy availability constrain the development of large brains, predicting that brain size correlates with the duration of maternal investment and with maternal basal metabolic rate (BMR) (11,12).…”

“…First, life history correlates could reflect the benefits of large brains in providing a "cognitive buffer" against environmental unpredictability, improving survival and permitting long lives (2,6,7). Second, selection on brain size might have secondary consequences for life history because larger brains impose a developmental cost in terms of a need for extended growth and maturation (3)(4)(5)8).…”

A battle over brains

“…This is essentially the extreme case of a theory proposed in this issue by Karin Isler [1], based on identifying a link between basal metabolic rate (BMR) and brain size: a necessary energetic flexibility to cope with extreme environmental variations, it is claimed, sets an upper limit on brain size, the ''Grey Ceiling'', brain size in general being positively correlated with BMR. But important parts of that paper disagree -for example in the case of marsupial brains -with a recently proposed theory explaining brain size on the basis of constraints on maternal input, the so-called ''Neonatal Maturity Hypothesis'' (NMH), published in PNAS last year by Vera Weisbecker and Anjali Goswami [2].…”