Friends of friends: are indirect connections in social networks important to animal behaviour?

Abstract

Friend of a friend relationships, or the indirect connections between people, influence our health, well-being, financial success and reproductive output. As with humans, social behaviours in other animals often occur within a broad interconnected network of social ties. Yet studies of animal social behaviour tend to focus on associations between pairs of individuals. With the increase in popularity of social network analysis, researchers have started to look beyond the dyad to examine the role of indirect connections in animal societies. Here, I provide an overview of the new knowledge that has been uncovered by these studies. I focus on research that has addressed both the causes of social behaviours, i.e. the cognitive and genetic basis of indirect connections, as well as their consequences, i.e. the impact of indirect connections on social cohesion, information transfer, cultural practices and fitness. From these studies, it is apparent that indirect connections play an important role in animal behaviour, although future research is needed to clarify their contribution.

Keywords: cooperation; culture; fitness; heritability; indirect exchange; social brokers; social learning; social network analysis.

Figure 1

Direct and indirect connections in animal social networks. Social interactions occur in a polyadic network of social ties in gregarious species such as (a) rhesus macaques, Macaca mulatta, and (b) killer whales, Orcinus orca. Indirect connections can emerge from a number of different types of association, including (a) grooming and (b) nearest-neighbour proximity. In both (a) and (b), the individual on the far left is indirectly connected to the individual on the far right via their mutual direct connections to the individual in the middle. Direct and indirect connections can be represented graphically in social networks, whereby nodes are connected via lines representing associations. Here, grey nodes represent individuals that are connected to each other directly or indirectly (c). Together, direct and indirect connections can result in every actor being connected to every other actor in a population. In the cartoon network (d), the black node is connected to all other nodes, with node darkness decreasing as social distance to the black node increases. Photos: L. J. N. Brent.

Figure 2

Toy networks representing some of the most commonly used individual-based measures of indirect connectedness. Focal individuals are grey nodes. In each case, scores increase from left to right: the grey node in the right-most network has the highest score for a given measure. These are examples of measures based on unweighted and undirected associations, although weights and directions can be applied to most measures. Descriptive definitions of each measure are given in Table 1.

Figure 3

The genetic basis of indirect connections. The extent to which individuals are indirectly connected to others via affiliative interactions is not heritable in (a) yellow-bellied marmots (data from Brent, Heilbronner, et al., 2013), but is heritable in (b) humans (reprinted with permission from Fowler et al., 2009) and (c) rhesus macaques (data from Lea et al., 2010). Networks are based on grooming, play, co-foraging, greetings, spatial proximity and inspections in marmots, named friendships in humans, and grooming in rhesus macaques. Nodes represent individuals; lines represent interactions between pairs of individuals. In the rhesus macaque network (c), circles denote adult males, squares denote adult females, and red symbols denote individuals with the rare allele for two gene variants in the serotonin pathway and low eigenvector centrality.

Figure 4

Fitness consequences of indirect connections. Indirect connections were significant predictors of the probability of (a) an increase in rank in manakins (data from Brent, Heilbronner, et al., 2013), (b) infant survival in rhesus macaques (data from McDonald, 2007) and (c) survival in juvenile male bottlenose dolphins (reprinted with permission from Stanton & Mann, 2013). In (b), the inset graph shows infant survival for males (dashed line) and females (solid line).

Figure 5

The maintenance of cooperation by direct and indirect interactions. In direct exchange, individuals cooperate with those from whom they have received cooperative acts. In generalized indirect exchange, individuals cooperate with others if they have previously received cooperative interactions from anyone: A (lower open dot) cooperates with B (solid dot), and then B cooperates with others (upper open dot). In reputation-based indirect exchange, individuals cooperate with the individuals who cooperate with others: individual A (solid dot) cooperates with B (upper open dot), which results in C (lower open dot) cooperating with A.