Cascading indirect genetic effects in a clonal vertebrate

Abstract

Understanding how individual differences among organisms arise and how their effects propagate through social groups are fundamental questions in behavioral biology. Genetic variation among social partners can influence individual phenotypes, creating individual differences that might then have cascading effects in social groups. Using a clonal species, the Amazon molly (Poecilia formosa), we test the hypothesis that such indirect genetic effects (IGE) propagate beyond individuals that experience them firsthand. We tested this hypothesis by exposing genetically identical Amazon mollies to social partners of different genotypes, and then moving these individuals to new social groups in which they were the only member to have experienced the IGE. We found that the differences in aggression experienced in genetically different social environments carried over into new social groups to influence the exploratory behaviors of individuals that did not directly experience the previous social environments. Our data reveal that IGE can propagate beyond the individuals that directly experience them in Amazon mollies and possibly in many group-living species. Theoretical and empirical expansion of the quantitative genetic framework developed for IGE to include cascading and other types of carry-over effects will facilitate understanding of among-individual variation, social behavior and its evolution.

Cascading indirect genetic effects in a clonal vertebrate

“…All data are archived on figshare (doi:10.6084/m9.figshare.1961506210.6084/m9.figshare.19615062). Electronic supplemental material is available online [66].…”

Indirect genetic effects for social network structure in Drosophila melanogaster

“…Theoretical and empirical work incorporating IGEs has seeded a better understanding of variation in social interactions and social dynamics [10–14]. However, models of IGEs have struggled to move beyond dyadic social interactions, to better mimic the common natural situation in which many individuals (and their genotypes and phenotypes) interact simultaneously [4,5,14–17]. This limitation is problematic for applying IGE theory to data from wild study systems, because individuals frequently engage in social interactions with multiple conspecifics, either simultaneously or sequentially.…”

“…To move beyond studying IGEs in dyadic contexts, social network analysis provides a promising opportunity, as it allows us to measure how the effects of social group members cascade through networks of direct and indirect interactions [4–6,17]. Social network analysis has emerged as a widely used tool for describing how individuals' direct and indirect social interactions are nested within the emergent social structure of their group [1,2,31–34], but has only rarely been deployed in genetically informative samples that would allow estimation of IGEs [4,5,17].…”

“…Extending our knowledge of how the genetic effects of social group members affect the structure and dynamics of networks of social interactions—i.e. IGEs within social networks—can allow us to better understand how variation in social structures forms, shapes behaviour and its genetic basis, and evolves [3–5,17].…”

“…As such, while the hypothesis that the genotypic composition of social groups should influence individuals' network positions seems intuitive, this is not a guarantee; and empirical evidence evaluating the effects of IGEs in social networks (or their absence) is lacking. Indeed, few studies have addressed how an individual's own genotype influences its position within a social network [37,44–46], and we know even less about how the genotypic composition of social groups and IGEs of interacting group members shape variation in network phenotypes [5,17,40]. A handful of studies have addressed how the genotypic makeup of a social group impacts various aspects of its structure and dynamics: social niche construction [28,47–49], exploratory behaviour [26], collective foraging [50], antipredator behaviour [10] and aggression [15,38].…”