The observed trade-off between the maximum rate of population increase (rmax
) and both absolute and relative brain size supports the notion that this trade-off is caused by an energetic constraint, especially since it disappears in lineages where the mother's energetic burden during reproduction is alleviated through helpers. Thus, our results fully support the expensive brain hypothesis, which predicts that relatively large brains can evolve only when either energy input increases (Isler & Van Schaik 2006b
) or there is an allocation shift from another expensive body function, such as production, or the size of an expensive tissue, such as the digestive tract in primates (Aiello & Wheeler 1995
) or the pectoral muscle in birds (Isler & Van Schaik 2006a
). To our knowledge, this framework is the only one that accounts for the well-known correlation between life-history patterns and brain size (reviewed in Deaner et al. 2003
; Barrickman et al. 2008
), while at the same time incorporating the energetic consequences of lifestyles that are influenced by ecological conditions of habitat and diet.
The rmax–brain size trade-off indicates that there is a maximum viable brain size for a species (its grey ceiling), beyond which viable populations cannot be sustained. The rate rmax represents the ability of a species to recover from population crashes due to starvation, disease or other evolutionary disasters, and therefore indexes the risk of local extinction. In species with low rmax, temporarily high rates of mortality are not easily buffered, so genetically based adaptation to environmental changes is hindered owing to the very limited room for selective mortality. Although it is impossible to pinpoint the exact value of this grey ceiling for any given lineage, it should depend on the stability of the habitat and the species' ability to buffer itself from such fluctuations, and thus its lifestyle. We assume that extant great ape species are very close to the absolute minimum viable rmax, and thus to the grey ceiling for primates. A similar value may apply to cetaceans, although valid estimates of maximum lifespan are notoriously difficult to obtain for these animals. In other lineages that are neither arboreal nor oceanic, the threshold may be considerably higher, as they may more often suffer from periodic population crashes.
These analyses demonstrate that at least in the precocial mammals and birds examined here, brain size, rather than body size, drives the value of rmax
, and therefore a species' extinction risk. Thus, we propose that the historical pattern of species extinctions, generally attributed to large body size (Brook & Bowman 2005
; but see Pimm et al. 1988
), is instead at least partly driven by large brain size. Despite substantial benefits of enhanced cognitive abilities (e.g. Sol et al. 2007
), we therefore predict that during mass extinctions large-brained taxa are especially vulnerable. On a macroevolutionary time scale, homoeothermic vertebrates tend to increase their brain size (but not in reptiles: Jerison 1969
). Owing to the rmax
–brain size trade-off, reproductive capacity decreases at the same time, leading taxa to a ‘drift’ towards ever-lower rmax
. Over evolutionary time, we therefore also predict that lineages will tend to evolve towards a maximum sustainable brain size, and that every clear increase in brain size beyond their grey ceiling is accompanied by a significant change in lifestyle (usually accompanied by the emergence of a new lineage).
But what change of lifestyle would allow the evolution of larger brained lineages? Our results show that, as predicted by the expensive brain hypothesis, allomaternal energy inputs during offspring production are one critically important factor. In lineages in which mothers are helped, such as altricial birds or canid carnivores, the rmax–brain size trade-off is not found. This means that allomaternal care enables species to increase their brain size without compromising their demographic viability. More generally, we propose that extensive allomaternal care will allow brain size, and thus also cognitive abilities, to increase relative to their independently breeding relatives when conditions favour this.
This also explains why there are many lineages of birds that independently evolved relatively large brains (Nealen & Ricklefs 2001
), but only a few in mammals (for phylogenetic analyses, see the electronic supplementary material). For 127 bird families from 23 orders, the upper 10 per cent quantile of brain mass residuals contains 13 families in seven different orders (Bucerotiformes, Psittaciformes, Piciformes, Strigiformes, Passeriformes and Ciconiiformes), all of which are altricial or semi-altricial. On the other hand, for 109 eutherian mammal families from 18 orders, the upper 15 per cent quantile of brain mass residuals contain 16 families in only two orders (Cetacea and Primates). In the absence of systematic comparisons, we draw attention to one spectacular example, Homo sapiens
(see Van Schaik & Isler submitted
). Humans have evolved allomaternal provisioning of offspring and allocare among adults, especially for the benefit of reproducing females (Hrdy 2005
), and increased brain size approximately threefold relative to their sister group, the genus Pan