Detecting Cryptic Indirect Genetic Effects

Abstract

Indirect genetic effects (IGEs) occur when genes expressed in one individual alter the phenotype of an interacting partner. IGEs can dramatically affect the expression and evolution of social traits. However, the interacting phenotype(s) through which they are transmitted are often unknown, or cryptic, and their detection would enhance our ability to accurately predict evolutionary change. To illustrate this challenge and possible solutions to it, we assayed male leg-tapping behavior using inbred lines of Drosophila melanogaster paired with a common focal male strain. The expression of tapping in focal males was dependent on the genotype of their interacting partner, but this strong IGE was cryptic. Using a multiple-regression approach, we identified male startle response as a candidate interacting phenotype: the longer it took interacting males to settle after being startled, the less focal males tapped them. A genome-wide association analysis identified approximately a dozen candidate protein-coding genes potentially underlying the IGE, of which the most significant was slowpoke. Our methodological framework provides information about candidate phenotypes and candidate single-nucleotide polymorphisms that underpin a strong yet cryptic IGE. We discuss how this approach can facilitate the detection of cryptic IGEs contributing to unusual evolutionary dynamics in other study systems.

Indirect genetic effects in behavioral ecology: does behavior play a special role in evolution?

“…Earlier work also used experimental evolution in lines of D. serrata to demonstrate evolution of ψ for sexually-selected cuticular hydrocarbon profiles (Chenoweth et al 2010). In D. melanogaster, a multiple regression approach was used with 50 interacting, inbred lines from the Drosophila Genetic Resource Panel to identify candidate interacting traits affecting focal male tapping behavior, which was demonstrated to be affected by IGEs but required interrogation to identify traits involved with the IGE (Bailey and Hoskins 2014). While there is clearly heterogeneity in the approach for manipulating the genotype of interacting individuals in such studies, the use of a common, standardized estimator allows comparison of the relative importance of IGEs across different species, traits and contexts.…”

“…For example, IGEs on growth in pigs arising from behavioral phenotypes such as aggressive biting are not only documented, but have been successfully selected in artificial breeding programs (Camerlink et al 2013(Camerlink et al , 2014. In contrast, isogenic focal Drosophila melanogaster males vary in how much they physically tap interacting partners of different genotypes with their prothoracic legs during bouts of interaction lasting only minutes, a behavior that might reflect gustatory sampling or aggression (Bailey and Hoskins 2014). Not only the timing of socially plastic responses underlying IGEs, but when during life any fitness effects of those changes are manifested, will ultimately impact evolutionary dynamics shaping behavior (Schneider et al 2017).…”

“…A combined trait-based and variance partitioning approach identified a behavioral trait, the startle response, as a possible mediator of this IGE (Bailey and Hoskins 2014).…”

Social structure and indirect genetic effects: genetics of social behaviour

“…(8) We are seeing progress in determining interactive phenotypes which are affected by the social environment ['group' to individual ] and interactive phenotypes that are determined between individuals [individual to individual (Penn et al, 2010;Bailey & Hoskins, 2014)]. Our hope is that molecular, physiological and quantitative approaches not only continue to investigate the effects of being 'social', but also converge to create an integrative social paradigm.…”

“…Note that z 1 and z 2 are not necessarily the same phenotype, and may need exploratory analysis (such as multiple regressions) to identify them (Bailey & Hoskins, 2014). Revealing such correlation(s) leads to a more comprehensive understanding of heritable behavioural regulation, including cell and molecular pathway(s) underlying the socially influential phenotype (z 2 ), and also the pathway(s) involved in the reception and integration of the social surrounding ( ).…”