Minimal variation in eutherian brain growth rates during fetal neurogenesis

Abstract

A central question in the evolution of brain development is whether species differ in rates of brain growth during fetal neurogenesis. Studies of neonatal data have found allometric evidence for brain growth rate differences according to physiological variables such as relative metabolism and placental invasiveness, but these findings have not been tested against fetal data directly. Here, we measure rates of exponential brain growth acceleration in 10 eutherian mammals, two marsupials, and two birds. Eutherian brain acceleration exhibits minimal variation relative to body and visceral organ growth, varies independently of correlated growth patterns in other organs, and is unrelated to proposed physiological constraints such as metabolic rate or placental invasiveness. Brain growth rates in two birds overlap with eutherian variation, while marsupial brain growth is exceptionally slow. Peak brain growth velocity is linked in time with forebrain myelination and eye opening, reliably separates altricial species born before it from precocial species born afterwards, and is an excellent predictor of adult brain size ( = 0.98). Species with faster body growth exhibit larger relative brain size in early ontogeny, while brain growth is unrelated to allometric measures. These findings indicate a surprising conservation of brain growth rates during fetal neurogenesis in eutherian mammals, clarify sources of variation in neonatal brain size, and suggest that slow body growth rates cause species to be more encephalized at birth.

Rediscovering and Reviving Old Observations and Explanations of Metabolic Scaling in Living Systems

“…If a functional link exists between brain mass and metabolic rate, it may only occur in eutherian mammals, which have long periods of placental nutrient provisioning of offspring [202]. Furthermore, this possible link may involve an effect of maternal metabolic rate (and thus rate of energy provisioning) on neonatal brain growth ( [205][206][207]; but see [208]), rather than a direct effect of the high-energy use of the adult brain on metabolic rate, as suggested by some investigators (e.g., [106,192,200,209]. This hypothesis is consistent with a lack of a positive correlation between body-size adjusted metabolic rate and adult brain mass in animal taxa without prolonged intrauterine development, including birds [210], marsupials [202,211] and teleost fishes [212,213], which also contradicts the models of [106,192].…”

Developmental duration as an organizer of the evolving mammalian brain: scaling, adaptations, and exceptions

“…In general, the ordering of developmental events, within and across systems, varies little, but there are several notable exceptions. For most eutherian mammals, however, rates of developmental processes are quite similar (Halley, 2017). Rates of particular processes may vary considerably between taxonomic groups-for example, considering the entire brain, marsupials generate neurons more slowly per unit time than do primates, rodents, or carnivores (Darlington, Dunlop, & Finlay, 1999).…”

Craniofacial skeletal response to encephalization: How do we know what we think we know?

“…Peak brain growth velocity is achieved just prior to birth (Halley, 2017), with human neonatal brain weights averaging approximately 360–380 g (Dekaban & Sadowsky, 1978; DeSilva & Lesnik, 2008; Ho, Roessmann, Hause, & Monroe, 1981). Brain growth continues postnatally, but follows a decelerating decay curve (Halley, 2017; Halley & Deacon, 2017). Maximum brain weight and high rates of synapse formation, myelination, and dendritic development are reached during postnatal life, while gradual declines in weight begin around age 45–50 (de Graaf-Peters & Hadders-Algra, 2006; Dekaban & Sadowsky, 1978).…”

“…Due to a slightly longer gestational period in humans relative to chimpanzees, at least part of the difference in absolute neonatal brain size can be attributed to the longer duration of prenatal brain growth, although the main contributor to the larger human neonatal brain is a faster prenatal rate of growth (Neubauer, 2015). Postnatal growth also contributes to the unique degree of human encephalization, whether through species-specific differences in postnatal growth grates or an extended duration of human postnatal brain growth (Halley, 2017; Halley & Deacon, 2017; Leigh, 2004; Passingham, 1985). However, it is the prenatal growth of the human brain that provides the foundation for initial skull formation and growth.…”