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 (np = 12) and nonprimate (nnp = 16) mammalian species, and was complemented by later ontogenetic data in 16 additional species (np = 9; nnp = 7) as well as neonatal proportions in a much larger sample (np = 38; nnp = 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.

1.
Barton RA, Capellini I (2011): Maternal investment, life histories and brain growth in mammals. Proc Natl Acad Sci 108:6169-6174.
2.
Barton RA, Harvey PH (2000): Mosaic evolution of brain structure in mammals. Nature 405:1055-1058.
3.
Butler H, Juurlink BHJ (1987): An Atlas for Staging Mammalian and Chick Embryos. Boca Raton, CRC Press.
4.
Charnov EL, Berrigan D (1993): Why do female primates have such long lifespans and so few babies? Or life in the slow lane. Evol Anthropol 1:191-194.
5.
Cheek DB (1975): Appendix II: data on normal fetal and postnatal Macaca mulatta; in Cheek DB (ed): Fetal and Postnatal Cellular Growth. Hoboken, Wiley, pp 521-534.
6.
Clauss M, Dittmann MT, Müller DWH, Zerbe P, Codron D (2014): Low scaling of a life history variable: analysing eutherian gestation periods with and without phylogeny-informed statistics. Mamm Biol 79:9-16.
7.
Count EW (1947): Brain and body weight in man: their antecedents in growth and evolution. Ann NY Acad Sci 46:993-1122.
8.
Deacon TW (1990): Problems of ontogeny and phylogeny in brain-size evolution. Int J Primatol 11:237-282.
9.
Deacon TW (1997): The Symbolic Species. New York, WW Norton & Co.
10.
Dobbing J, Sands J (1979): Comparative aspects of the brain growth spurt. Early Hum Dev 3:79-83.
11.
Elliot MG, Crespi BJ (2008): Placental invasiveness and brain-body allometry in eutherian mammals. J Evol Biol 21:1763-1778.
12.
Forbes TL, Lopez GR (1989): Determination of critical periods in ontogenetic trajectories. Funct Ecol 3:625-632.
13.
Goedbloed JF (1976): Embryonic and postnatal growth of rat and mouse. IV. Prenatal growth of organs and tissues: age determination, and general growth pattern. Acta Anat 95:8-33.
14.
Gould S (1975): Allometry in primates, with emphasis on scaling and the evolution of the brain. Contrib Primatol 5:244-292.
15.
Gould SJ (1977): Ontogeny and Phylogeny. Cambridge, Harvard University Press.
16.
Halley AC (2015): Meta-analysis of ontogenetic brain/body allometry in mammals: implications for primate encephalization and fetal growth theories of relative brain size (abstract). Brain Behav Evol 85:289-290.
17.
Harvey PH, Clutton-Brock TH (1985): Life history variation in primates. Evolution 39:559-581.
18.
Herculano-Houzel S, Collins CE, Wong P, Kaas JH (2007): Cellular scaling rules for primate brains. Proc Natl Acad Sci USA 104:3562-3567.
19.
Holt AB, Cheek DB, Mellits ED, Hill DE (1975): Brain size and the relation of the primate to the nonprimate; in Cheek DB (ed): Fetal and Postnatal Cellular Growth: Hormones and Nutrition. Hoboken, Wiley, pp 23-44.
20.
Holt AB, Renfree M, Cheek D (1981): Comparative aspects of brain growth: a critical evaluation of mammalian species used in brain growth research with emphasis on the Tammar wallaby; in Hetzel BS, Smith RM (eds): Fetal Brain Disorders - Recent Approaches to the Problem of Mental Deficiency. Amsterdam, Elsevier/North-Holland Biomedical Press, pp 17-43.
21.
Jerison HJ (1973): Evolution of the Brain and Intelligence. New York, Academic Press.
22.
Kleiber M (1961): The Fire of Life: An Introduction to Animal Energetics. Hoboken, Wiley.
23.
Krubitzer L, Dooley JC (2013): Cortical plasticity within and across lifetimes: how can development inform us about phenotypic transformations? Front Hum Neurosci 7:620.
24.
Laird AK (1967): Evolution of the human growth curve. Growth 31:345-355.
25.
Leigh SR (2001): Evolution of human growth. Evol Anthropol 10:223-236.
26.
Leutenegger W (1973): Maternal-fetal weight relationships in primates. Folia Primatol 20:280-293.
27.
Leutenegger W (1979): Evolution of litter size in primates. Am Nat 114:525-531.
28.
MacLean EL, Hare B, Nunn CL, Addessi E, Amici F, Anderson RC, et al. (2014): The evolution of self-control. Proc Natl Acad Sci USA 111:E2140-E2148.
29.
Martin RD (1981): Relative brain size and basal metabolic rate in terrestrial vertebrates. Nature 293:57-60.
30.
Martin RD (1983): Human Brain Evolution in an Ecological Context. New York, American Museum of Natural History.
31.
Martin RD (1996): Scaling of the mammalian brain: the maternal energy hypothesis. Physiology 11:149-156.
32.
Pagel MD, Harvey PH (1988): How mammals produce large-brained offspring. Evolution 42:948-957.
33.
Payne PR, Wheeler EF (1968): Comparative nutrition in pregnancy and lactation. Proc Nutr Soc 27:129-138.
34.
Pontzer H, Raichlen DA, Gordon AD, Schroepfer-Walker KK, Hare B, O'Neill MC, Muldoon KM, Dunsworth HM, Wood BM, Isler K, Burkart J, Irwin M, Schumaker RW, Lonsdorf EV, Ross SR (2014): Primate energy expenditure and life history. Proc Natl Acad Sci USA 111:1433-1437.
35.
Preuss TM (2007): Evolutionary specializations of primate brain systems; in Ravosa MA, Dagosto M (eds): Primate Origins: Adaptations and Evolution. Boston, Springer US, pp 625-675.
36.
Renfree MB, Holt AB, Green SW, Carr JP, Cheek DB (1982): Ontogeny of the brain in a marsupial (Macropus eugenii) throughout pouch life. Brain Behav Evol 20:57-71.
37.
Sacher GA (1982): The role of brain maturation in the evolution of the primates; in Armstrong E, Falk D (eds): Primate Brain Evolution. New York, Springer, pp 97-112.
38.
Sacher GA, Staffeldt EF (1974): Relation of gestation time to brain weight for placental mammals: implications for the theory of vertebrate growth. Am Nat 108:593-615.
39.
Smaers JB, Dechmann DKN, Goswami A, Soligo C, Safi K (2012): Comparative analyses of evolutionary rates reveal different pathways to encephalization in bats, carnivorans, and primates. Proc Natl Acad Sci USA 109:18006-18011.
40.
Stephan H, Andy, OJ (1970): The allocortex in primates; in Noback CR, Montagna W (eds): The Primate Brain - Advances in Primatology. New York, Appleton Century Crofts, vol 1, pp 109-135.
41.
Streeter GL (1949): Developmental horizons in human embryos (fourth issue): a review of the histogenesis of cartilage and bone. Contrib Embryol 33:149-169.
42.
Striedter GF (2005): Principles of Brain Evolution. Sunderland, Sinauer Associates.
43.
Striedter GF, Charvet CJ (2008): Developmental origins of species differences in telencephalon and tectum size: morphometric comparisons between a parakeet (Melopsittacus undulates) and a quail (Colinus virgianus). J Comp Neurol 507:1663-1675.
44.
van Dongen P (1998): Brain size in vertebrates; in Nieuwenhuys R, ten Donkelaar HJ, Nicholson C (eds): The Central Nervous System of Vertebrates. New York, Springer, pp 2099-2131.
45.
Vinicius L (2005): Human encephalization and developmental timing. J Hum Evol 49:762-776.
46.
Widdowson EM (1981): Growth of creatures great and small. Symp Zool Soc Lond 46:5-17.
47.
Wingert F (1969): Biometrische Analyse der Wachstumsfunktionen von Hirnteilen und Körpergewicht der Albinomaus. J Hirnforschungen 11:133-197.
48.
Workman AD, Charvet CJ, Clancy B, Darlington RB, Finlay BL (2013): Modeling transformations of neurodevelopmental sequences across mammalian species. J Neurosci 33:7368-7383.
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