Indirect genetic effects for social network structure in Drosophila melanogaster

Abstract

The position an individual holds in a social network is dependent on both its direct and indirect social interactions. Because social network position is dependent on the actions and interactions of conspecifics, it is likely that the genotypic composition of individuals within a social group impacts individuals' network positions. However, we know very little about whether social network positions have a genetic basis, and even less about how the genotypic makeup of a social group impacts network positions and structure. With ample evidence indicating that network positions influence various fitness metrics, studying how direct and indirect genetic effects shape network positions is crucial for furthering our understanding of how the social environment can respond to selection and evolve. Using replicate genotypes of Drosophila melanogaster fruit flies, we created social groups that varied in their genotypic makeup. Social groups were videoed, and networks were generated using motion-tracking software. We found that both an individual's own genotype and the genotypes of conspecifics in its social group affect its position within a social network. These findings provide an early example of how indirect genetic effects and social network theory can be linked, and shed new light on how quantitative genetic variation shapes the structure of social groups. This article is part of a discussion meeting issue ‘Collective behaviour through time’.

Genetic variance and indirect genetic effects for affiliative social behavior in a wild primate

“…These findings are also consistent with evidence from human populations suggesting that loneliness and social integration are weakly to modestly heritable and subject to strong environmental effects, including IGEs (Day et al 2018, Abdellaoui et al 2019. IGEs for cooperative antipredator behavior have been documented laboratory guppies (Bleakley and Brodie 2009), for social network metrics in flies (Wice and Saltz 2023) and for maternal-offspring interactions in mice (Ashbrook et al 2015). However, the presence and magnitude of IGEs for affiliative social behaviors remains largely unexplored in wild animals.…”

Using a Combination of Novel Research Tools to Understand Social Interaction in the Drosophila melanogaster Model for Fragile X Syndrome

“…SNA has been used in the last 20 years to analyze collective animal behaviors and identify group SI patterns (reviewed in: [ 31 ]). There has also been a growing interest in utilizing SNA to examine the social behavior of D. melanogaster [ 16 , 18 , 22 , 24 , 26 , 31 , 32 , 33 , 34 ]. In addition, our study, for the first time, provides results of SI in the FXS model of fruit flies obtained using a combination of novel tools: the Drosophila Shallow Chamber and the open-source Python data processing pipeline for analysis of SI in D. melanogaster .…”

“…The importance of the current research on SI in the Drosophila FXS model is based on the fact that the social network structure is highly influenced by genotype [ 16 , 24 , 32 , 33 ]. Different D. melanogaster strains exhibit differences in SINs, indicating the potential influence of genes on SIN structure [ 32 ].…”

“…Betweenness centrality displayed the highest broad-sense heritability, with genotype accounting for about 17% of the variation in this network measure [ 24 ]. Additionally, Wice and Saltz (2023) demonstrated that SIN measures depend on the individual’s genotype and the genotypes of other individuals within the network [ 24 , 33 ]. Furthermore, Alwash et al (2021) investigated the characteristics of SI in flies mutated in for, a pleiotropic gene regulating several metabolic, physiological and behavioral phenotypes [ 32 ].…”

A multi-scale review of the dynamics of collective behaviour: from rapid responses to ontogeny and evolution

“…In some species without groups of stable membership, short-term studies can overcome this by testing the same individual with different groupmates. Wice & Saltz [ 182 ] exploit the powerful fruit fly system to generate replicated social groups to better investigate how social interactions among individuals influence entire social networks. Finding both direct and indirect genetic effects on an individual's social position within the network opens up the possibility for the evolution of the entire social environment.…”