Cascading Indirect Genetic Effects

Understanding cascading indirect genetic effects (IGE) in a unisexual species.

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. To distinguish this effect from first- and second-order IGE, we use the term 'cascading IGE'.

To address this idea of cascading IGE, I generate three different "typical IGE" social environments from these 3 clonal lineages. Focal females were placed into a social environment with two sister clones which we will call the Monoclonal social environment. Or with two partner females from Clone 1 or Clone 2. Females were exposed to these social environments for a total of three months. During this time, we measured aggressive behaviors among all 3 females. We choose to measure aggression as it is common in Amazon mollies and there is preliminary evidence that these 3 clonal lineages differ in the amount of aggression they display.

After four weeks we removed the focal females and placed her into a new social environment with two novel sister clones. This new environment will allow us to test the hypothesis of cascading IGE. Specifically, this approach allows us to measure how living in long-term social environments that vary in aggression can influence the exploratory / stress behaviors of that individual when placed into a novel environment. (I.e., how does living in a stressful environment influence exploratory stress behaviors in a new environment?)

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 social behavior and its evolution.

This inital study can be found in more detail on BioRxvi: Makowicz AM, Bierbach D, Richardson C*, Hughes KA. 2021. Cascading indirect genetic effects in a clonal vertebrate. BioRXiv preprint, doi: https://doi.org/10.1101/2021.02.27.433187.

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In a current follow up study we ask: If cascading IGE depend on the degree of genetic similarity between past and current social partners OR previous experience with genotypes?

Cascading IGE we find in the above study may depend on the degree of genetic similarity between past and current social partners. Thus, current research is now underway to discover if these cascading IGE depend on the degree of genetic similarity between past and current social partners. For instance, do cascading IGE only occur between like genotypes. Where we would find transmission of past IGE between sister clones only but not between focal females and clone 1 or clone 2 partner females regardless of the social experience she has experienced.

Or are cascading IGE dependent upon previous experience with genotypes? Their transmission may be dependent upon if the focal female has had previous interactions with a specific genome or not. If this were true, we would predict that cascading IGE would be transmitted differently when focal females are paired with sister clones compared to partner females from either clone 1 or clone 2 (with whom she has no prior experience with). But then in social environments where the focal female has experienced both sister clones and another clonal lineage (either clone 1 or 2), cascading IGE would be transmitted differently to the two genomes she has experience with compared to partner females from novel clonal lineage.

These are just some ways in which cascading IGE can influence phenotypic variation among individuals that live in fluid social environments.

This research was supported via a Postdoctoral fellowship from the Provost Postdoctoral Fellow Program and completed in collaboration with Dr. Kimberly Hughes at Florida State University.