Placental invasiveness and brain–body allometry in eutherian mammals

Abstract

Brain growth is a key trait in the evolution of mammalian life history. Brain development should be mediated by placentation, which determines patterns of resource transfer from mothers to fetal offspring. Eutherian placentation varies in the extent to which a maternal barrier separates fetal tissues from maternal blood. We demonstrate here that more invasive forms of placentation are associated with substantially steeper brain–body allometry, faster prenatal brain growth and slower prenatal body growth. On the basis of the physiological literature we suggest a simple mechanism for these differences: in species with invasive placentation, where the placenta is bathed directly in maternal blood, fatty acids essential for brain development can be readily extracted by the fetus, but in species with less invasive placentation they must be synthesized by the fetus. Hence, with regard to brain–body allometry and prenatal growth patterns, eutherian mammals are structured into distinct groups differing in placental invasiveness.

Does more maternal investment mean a larger brain? Evolutionary relationships between reproductive mode and brain size in chondrichthyans

“…Previous studies of placental (eutherian) mammals suggest that it is worth searching for such a link; more 'invasive' forms of placentation (haemochorial), with the closest connection between maternal and fetal blood supply, exhibit a steeper brain-body allometric relationship than does less invasive placentation (endochorial and epithiliochorial) (Elliot and Crespi 2008). Hence, larger haemochorial mammals have larger brains for a given body size than do those with other less tightly connected placentas.…”

“…The brain is perhaps the most energetically expensive organ to produce and maintain, and thus has been the subject of many allometric studies in mammals, birds and reptiles (Martin 1981(Martin , 1996Iwaniuk and Nelson 2001;Elliot and Crespi 2008;Isler and van Schaik 2009). Most studies have focussed on functional implications of brain size and the development of major brain regions in vertebrates, examining ecological or behavioural correlates with brain organisation (Barton et al 1995;Kotrschal et al 1998;Lefebvre et al 2002;Yopak et al 2007;Shumway 2008), whereas few have examined any potential physiological mechanisms that drive this diversity (Elliot and Crespi 2008).…”

“…Hence, larger haemochorial mammals have larger brains for a given body size than do those with other less tightly connected placentas. Elliot and Crespi (2008) proposed that the development of larger brains is facilitated by better embryonic access to maternally derived fatty acids, which are essential for the development of brain tissue; however, whether this is true of cartilaginous fishes remains unknown.…”

“…Comparative analyses in mammals (Elliot and Crespi 2008;Barton and Capellini, 2011) suggest suggest that higher levels of maternal investment will increase nutrient allocation to developing embryos, allowing increased growth of energetically expensive brain tissue. Our primary hypothesis is that variation in the relative brain size among chondrichthyans is directly related to reproductive mode.…”

“…Most studies have focussed on functional implications of brain size and the development of major brain regions in vertebrates, examining ecological or behavioural correlates with brain organisation (Barton et al 1995;Kotrschal et al 1998;Lefebvre et al 2002;Yopak et al 2007;Shumway 2008), whereas few have examined any potential physiological mechanisms that drive this diversity (Elliot and Crespi 2008). Much of neural development occurs during gestation and brain tissue accounts for a disproportionate amount of metabolic costs in early life (Martin 1996;Elliot and Crespi 2008), raising questions about the role of reproductive diversity, and the level of maternal investment in the evolution of relative brain sizes.…”