Allomaternal care, brains and fertility in mammals: who cares matters

Abstract

The expensive brain hypothesis predicts that the lowest stable level of energy input sets the upper limit to a species’ brain size. This prediction receives comparative support from the effects of experienced seasonality (including hibernation) and diet quality on mammalian brain size. Here, we test another prediction, which concerns the temporal stability of energy inputs. Allomaternal care in mammals can be provided by breeding males or other helpers (usually earlier offspring). Male care should be stable and reliable since otherwise no breeding would occur. Care by others, in contrast, should fluctuate, as the availability of helpers often varies. One would therefore predict, other things being equal, that the presence of male care in addition to maternal care should show positive correlated evolution with brain size, whereas care by others would not. However, because females can readily respond through litter size adjustments to variable amounts of energy inputs, helper inputs may be used to increase fertility. A detailed comparative analysis of a large sample of mammals (N = 478 species) showed that male help is correlated with the evolution of larger brains, whereas alloparental help is correlated with higher fertility, but only in species where male care is also present (as in cooperative breeders). Humans evolved an unusual form of multi-family cooperative breeding, which involves stable and reliable care by both fathers and alloparents. This combination helps to explain why humans differ from the other apes in having both an extremely large brain and a relatively high reproductive output.

Significance statement

Allomaternal care provides breeding females with energy, directly or indirectly, and so would be expected to affect fertility and/or brain size. Which path evolution actually took remains controversial, partly because previous studies did not separate between care provided by the breeding male (paternal care) and care by non-breeding helpers (alloparental care). We distinguish between them because we expect that selection only favours increased brain size if the increase in energy available to the female is predictable and constant. Using a sample of 478 mammals, we show that paternal care, which is both reliable and stable, shows correlated evolution with brain size, whereas alloparental care, which fluctuates with varying availability of helpers, is correlated with higher fertility. Thus, constraints on brain size, imposed by its high-energy costs, may predict brain size better than the fitness benefits of improved cognitive abilities per se.