Prenatal Brain-Body Allometry in Mammals

Abstract

Variation in relative brain size among adult mammals is produced by different patterns of brain and body growth across ontogeny. Fetal development plays a central role in generating this diversity, and aspects of prenatal physiology such as maternal relative metabolic rate, altriciality, and placental morphology have been proposed to explain allometric differences in neonates and adults. Primates are also uniquely encephalized across fetal development, but it remains unclear when this pattern emerges during development and whether it is common to all primate radiations. To reexamine these questions across a wider range of mammalian radiations, data on the primarily fetal rapid growth phase (RGP) of ontogenetic brain-body allometry was compiled for diverse primate (n_p = 12) and nonprimate (n_np = 16) mammalian species, and was complemented by later ontogenetic data in 16 additional species (n_p = 9; n_np = 7) as well as neonatal proportions in a much larger sample (n_p = 38; n_np = 83). Relative BMR, litter size, altriciality, and placental morphology fail to predict RGP slopes as would be expected if physiological and life history variables constrained fetal brain growth, but are associated with differences in birth timing along allometric trajectories. Prenatal encephalization is shared by all primate radiations, is unique to the primate Order, and is characterized by: (1) a robust change in early embryonic brain/body proportions, and (2) higher average RGP allometric slopes due to slower fetal body growth. While high slopes are observed in several nonprimate species, primates alone exhibit an intercept shift at 1 g body size. This suggests that primate prenatal encephalization is a consequence of early changes to embryonic neural and somatic tissue growth in primates that remain poorly understood.

Comparing adult hippocampal neurogenesis across species: translating time to predict the tempo in humans

“…confirmed the same notion (Halley, 2016(Halley, , 2017 In mammals, the onset of walking is predicted by neural maturation (which is conserved) 440…”

“…and related neuroplasticity are integrated with translating time in Finlay and Uchiyama 126 (2017), and finally, evolution of life histories, including events like weaning and 127 menopause in Hawkes and Finlay (2018). Readers are directed to the early work of 128 Passingham (1985), and Garwicz et al (2009), who use similar methods to examine 129 early independent ambulation, as well as that of Halley's studies of the growth of initial 130 primordia and brain across a wide range of mammals (Halley, 2016(Halley, , 2017 stages of hippocampal neurogenesis across species. 136 137 1.1.2 Allometry of brain and brain parts.…”

Minimal variation in eutherian brain growth rates during fetal neurogenesis

“…This makes total gestation length a poor marker for the variable of interest, namely the elapsed time from the onset of neurodevelopment (electronic supplementary material, figure S2a,b). Second, species differ in the timing of birth relative to peak velocity [10] (electronic supplementary material, figure S2c,d) and allometric brain/body growth [22] (electronic supplementary material, figure S3a), making birth a particularly unreliable proxy for fetal brain growth patterns. This has led several authors to directly caution against the use of birth as a temporal anchor in comparative neurodevelopment [23][24][25].…”

Interspecific comparison of allometry between body weight and chest girth in domestic bovids

“…However, White and Gould 3 emphasised the significance of the allometric intercept in ontogenetic and phylogenetic changes and as a taxonomic indicator. In recent, Halley 4 pointed out that the allometric intercept represents prenatal brain mass at 1 gram of body mass and it corresponds to a timing where most mammalian fetuses transit from embryonic to fetal development.…”