Heritable victimization and the benefits of agonistic relationships

Abstract

Here, we present estimates of heritability and selection on network traits in a single population, allowing us to address the evolutionary potential of social behavior and the poorly understood link between sociality and fitness. To evolve, sociality must have some heritable basis, yet the heritability of social relationships is largely unknown. Recent advances in both social network analyses and quantitative genetics allow us to quantify attributes of social relationships and estimate their heritability in free-living populations. Our analyses addressed a variety of measures (in-degree, out-degree, attractiveness, expansiveness, embeddedness, and betweenness), and we hypothesized that traits reflecting relationships controlled by an individual (i.e., those that the individual initiated or were directly involved in) would be more heritable than those based largely on the behavior of conspecifics. Identifying patterns of heritability and selection among related traits may provide insight into which types of relationships are important in animal societies. As expected, we found that variation in indirect measures was largely explained by nongenetic variation. Yet, surprisingly, traits capturing initiated interactions do not possess significant additive genetic variation, whereas measures of received interactions are heritable. Measures describing initiated aggression and position in an agonistic network are under selection (0.3 < |S| < 0.4), although advantageous trait values are not inherited by offspring. It appears that agonistic relationships positively influence fitness and seemingly costly or harmful ties may, in fact, be beneficial. Our study highlights the importance of studying agonistic as well as affiliative relationships to understand fully the connections between sociality and fitness.animal model | animal social networks | yellow-bellied marmots B ehavioral ecologists have long viewed sociality and social relationships as adaptive traits shaped by evolution (1, 2). However, if we are to study the evolution of sociality and social relationships, there must be heritable variation in traits describing individual social behavior. Numerous studies have identified heritable variation in animal dispositions (3, 4), morphological characteristics, and behavioral traits (5) that may affect how individuals interact with conspecifics, yet the role of genetics in social interactions themselves is poorly understood. If traits affecting social interactions are heritable, we may expect measures of social relationships to be explained somewhat by additive genetic factors.There has been a recent upsurge in using animal social networks as tools for studying the ecology, evolution, and adaptive significance of sociality (6-8). Networks are based on interactions between individuals, and a variety of measures have been developed to quantify how connected individuals are with others in the group (9). Although studies of nonhuman species have explored the development of social networks (10) as well as the causes (11-13) and...

Ontogenetic variation of heritability and maternal effects in yellow-bellied marmot alarm calls

“…Thus, many animals find themselves in multi-age groups comprising relatives. Social groups and social group membership are known [49]. Detailed methods of marmot trapping and marking can be found in a paper by Armitage [50].…”

“…We constructed a molecular genealogy where we used 12 microsatellite loci to determine maternity and paternity (details in [49,51]). Using the animal model [45,46], as implemented by ASREML [52], we decomposed the variance of alarm calls into its additive genetic, permanent environment (environmental effects on an individual's phenotype that are constant across repeated measures on that individual [53]), maternal environment (the effects on offspring phenotype that are shared by offspring of the same mother [53]), year and event (which reflects the consistency of calls during one recording event) components.…”

Social niche specialization under constraints: personality, social interactions and environmental heterogeneity

“…Gathering this type of data over different habitats, or differing social systems, or according to the frequency of certain social roles may greatly advance our understanding of social niche specialization and personality differences. Alternatively, Lea et al [18] studied the quantitative genetics of individuals' social network indices (i.e. out-degree, in-degree, attractiveness, expansiveness, embeddedness and betweenness) in a yellow-bellied marmot (Marmota flaviventris) population.…”

“…In addition to classical indices used in niche specialization studies [16], one could estimate the repeatability of the frequency of each type of social interactions in a population, or could use social network analyses indices (e.g. degree or betweeness) to characterize how individuals in a population differ in their social interactions [18]. Social niche specialization may also be considered as a particular facet of the overall ecological niche specialization if both have coevolved together.…”

Yellow-bellied marmots: insights from an emergent view of sociality

“…We capitalized on a wellsupported genetically based genealogy [43] and our ability to calculate a variety of social network statistics on the marmots. Using the quantitative genetic methods of 'the animal model' [84], we partitioned out components of variation and estimated additive genetic variation in social attributes [76].…”