The nature of privilege: intergenerational wealth in animal societies

The nature of privilege: intergenerational wealth in animal societies. Jennifer E Smith, B Natterson-Horowitz, Michael E Alfaro. Behavioral Ecology, arab137, December 7 2021. https://doi.org/10.1093/beheco/arab137

Abstract: Wealth inequality is widespread across human societies, from pastoral and small-scale agricultural groups to large modern social structures. The intergenerational transfer of wealth privileges some individuals over others through the transmission of resources external to an individual organism. Privileged access to household wealth (e.g., land, shelter, silver) positively influences the destinies of some (and their descendants) over others in human societies. Strikingly parallel phenomena exist in animal societies. Inheritance of nongenetic commodities (e.g., a nest, territory, tool) external to an individual also contributes greatly to direct fitness in animals. Here, we illustrate the evolutionary diversity of privilege and its disparity-generating effects on the evolutionary trajectories of lineages across the Tree of Life. We propose that integration of approaches used to study these patterns in humans may offer new insights into a core principle from behavioral ecology—differential access to inherited resources—and help to establish a broad, comparative framework for studying inequality in animals.

Intergenerational transfer of material wealth within family lineages

Intergenerational transfer of material wealth can drive inequality within family lineages of animals. In North American red squirrels (Tamiasciurus hudsonicus), a mother may store spruce cones on her territory and privilege her daughter by bequeathing a rich territory to her; daughters who receive these resources survive longer and reproduce earlier than those without (Smith 1968). Male food hoarders can also influence the lifetime fitness of subsequent owners of middens and these effects persist across multiple owners (Fisher et al. 2019). Because these food hoards outlive their owners, these indirect effects alter the environments that others experience. Thus, when some offspring receive a cone stash and others do not, this perpetuates inequality across generations privileging some individuals over others. Whereas many species, including the red squirrels described here, modify their local resource distributions (Laland et al. 1999; Olding-Smee 2012), studying the evolutionary dynamics associated with the intergenerational transfer of these constructed niches requires explicit study within a comparative framework.

The material transfer of (nongenetic) material wealth contributes to the extinction (vs. expansion) of family lineages and advantage individuals of the philopatric (vs. dispersing) sex across species. For spotted hyenas (Crocuta crocuta), individuals from multiple maternal lineages join forces to defend a shared territory, but high-born philopatric females and their descendants have privileged access to resources within them (Holekamp et al. 2012) (Figure 2). Differential access promotes the extinction of nonprivileged family lineages but expands land ownership by privileged animals; these effects are further ameliorated by differential access to social support within groups (Smith, Van Horn, et al. 2010; Strauss and Holekamp 2019). In contrast, territory acquisition by a young male red grouse (Lagopus lagopus scotica) is impacted by paternal presence (Watson et al. 1994) (Figure 2). Philopatric sons with nearby fathers gain larger and more defended territories than individuals whose fathers are no longer alive. Thus, the comparative study of wealth transfer across animals should therefore offer insights into the evolutionary dynamics of family groups and the consequences of sex-biased dispersal in animals.

The transgenerational use of activity sites can also contribute to the accumulation of stone tools within lineages. Taï Chimpanzees (Pan troglodytes verus) (Mercader et al. 2002) and bearded capuchin monkeys (Cebus libidinosus) (Elisabetta et al. 2013) inherit tools produced at nut-cracking sites via the paternal and maternal lines, respectively. Individuals that inherit are advantaged over others who do not in terms of their ability to gain access to key food resources; these beneficial effects are further compounded through the transfer of social information (e.g., traditions for how to use inherited materials) across generations. These examples shed light on the direct and indirect role of wealth transfer in shaping legacies of inequality along bloodlines over multiple time scales. These effects of intergenerational wealth mobility are likely stronger for some species than for others, as we discuss below, and therefore should be the subject of a quantitative study by behavioral ecologists to understand the breadth of their influence.

Intergenerational transfer of material wealth among non-kin

Intergenerational transfer of material wealth is not limited to genetic relatives within animal societies and can impose similar disparity-generating effects through preferential treatment by non-kin. For instance, privileged access to shelter (e.g., a nest) can transcend bloodlines in European paper wasps (Polistes dominula). Inheritance of built structures from kin or non-kin advantage wasps fortunate enough to receive them (Leadbeater et al. 2011). As a result, females who share nests with others are more likely to inherit structures and produce offspring than less privileged lone females. Within some termite societies structures may be inherited from kin, but inheritance can also occur when different lineages merge to share “real estate” (Thorne et al. 2003). The merging of families accelerates inheritance, increasing opportunities for resource acquisition for future generations, benefiting some termite lineages over others to further perpetuate the cycle of privilege. In some cases, disadvantaged individuals wait for privileged individuals to perish, as occurs, for example, in the clown anemonefish (Amphiprion percula) which lives in groups composed of non-relatives (Buston 2004). The non-breeding fish queue to inherit high-quality anemones from non-kin, but not all individuals inherit, and these effects can compound across multiple generations. Further inquiry into understanding selective processes shaping resource transfer among non-kin within a comparative perspective could offer new insights into the evolutionary origins of cooperation among non-relatives.