Who was helping? The scope for female cooperative breeding in early Homo

Abstract

Derived aspects of our human life history, such as short interbirth intervals and altricial newborns, have been attributed to male provisioning of nutrient-rich meat within monogamous relationships. However, many primatologists and anthropologists have questioned the relative importance of pair-bonding and biparental care, pointing to evidence that cooperative breeding better characterizes human reproductive and child-care relationships. We present a mathematical model with empirically-informed parameter ranges showing that natural selection favors cooperation among mothers over a wide range of conditions. In contrast, our analysis provides a far more narrow range of support for selection favoring male coalition-based monogamy over more promiscuous independent males, suggesting that provisioning within monogamous relationships may fall short of explaining the evolution of Homo life history. Rather, broader cooperative networks within and between the sexes provide the primary basis for our unique life history.

Figure 1. Infant care classification for 105 primate species, from the appendix to Sarah Hrdy’s treatise on infant care , .

Hrdy’s classification follows: Exclusive maternal care: mother is very possessive and is the only one to hold and carry her infant. Maternal and paternal care: mother allows male she is paired with to take and carry infant and he is eager to do so. In New World monkeys, infant may actually take the initiative in transferring to “father.” Typically, the mother’s mate is the main caretaker, and alloparents are rarely involved. Shared care: mother is tolerant and allows allomothers to take and carry her infant within 3 weeks of birth. Shared care with suckling: group members other than the mother care for infants, and if the allomother is lactating, she allows an infant other than her own to suckle. Allomaternal suckling may range from occasional and brief access to more sustained access, as in species where two mothers share a nest. Shared care + prov: provisioning ranges from minimal to extensive. Shared care + milk + provisioning: combinations of behaviors described above.

Figure 2. Model analysis illustrating the scope for cooperative mothers.

The upper row describes a deterministic process of the evolutionary dynamics of the three female strategies: Independent Mother (IM), Opportunistic Mother (OM), and Cooperative Mother (CM). The gray region is when selection favors CM, white region is when OM is favored, and the thicker dark line is where the fitness of OMs and IMs are the same. Panels (a)–(c) assume parameter values , , , , , , and . However panel (a) assumes no kin selection () and panel (b) prescribes weak kin selection (), and panel (c) specifies strong kin selection (). The bottom row of panels describes the basin of attraction for Cooperative Mothers through stochastic simulation as a function of the repeated interaction parameter (panel (d)), level of kin selection (panel (e)), and the effect of alloparental care (panel (f)). The position of the unstable equilibrium between OM and CM females shown in the ternary plots above defines the basin of attraction. The dashed curves are 95% confidence bounds around the mean (solid line) computed by taking 1000 random uniform parameter values within the ranges reported in Table 1 for each value of , , and on the horizontal axis for panels (d)–(f), respectively.

Figure 3. Plot of the fitness differences between Coalition Males () and Non-coalition Males () as a function of the differences in the level of Extra-Pair Matings (EPMs) and childcare.

For the left panel the level of EPMs for Coalition Males is set at . The right panel has the level of paternal care for Non-coalition Males set at . The solid line with its respective confidence intervals (dashed lines) were estimated through simulation by drawing 10,000 random parameter sets from Table 1. Gray regions highlight when Coalition Males are favored, with the corresponding white region showing when Non-coalition Males are favored. The level of kin selection () and positive assortment between Cooperative Mothers and Coalition Males () is zero.

Figure 4. Kin selection, male-female cooperative assortment and density-dependent evolutionary dynamics of Coalition Males.

For all panels, each frequency of Cooperative Mothers () and Coalition Males (), 100 parameter sets were randomly drawn from ranges in Table 1 to estimate the distribution of when the fitness of Coalition Males is greater than that of Non-coalition Males (). Dark regions indicate when the mean of those distributions at a specific value of and favor Coalition Males. The level of kin selection () is the same across panel rows and the level of positive assortment between Cooperative Mothers and Coalition Males () is the same within a column of panels.