The March of the Beetles: Epistatic Components Dominate Divergence in Dispersal Tendency in Tribolium castaneum

Abstract

The genetic underpinnings of traits are rarely simple. Most traits of interest are instead the product of multiple genes acting in concert to determine the phenotype. This is particularly true for behavioral traits, like dispersal. Our investigation focuses on the genetic architecture of dispersal tendency in the red flour beetle, Tribolium castaneum. We used artificial selection to generate lines with either high or low dispersal tendency. Our populations responded quickly in the first generations of selection and almost all replicates had higher dispersal tendency in males than in females. These selection lines were used to create a total of six additional lines: F1 and reciprocal F1, as well as four types of backcrosses. We estimated the composite genetic effects that contribute to divergence in dispersal tendency among lines using line cross analysis. We found variation in dispersal tendency of our lines was best explained by autosomal additive and three epistatic components. Our results indicate that dispersal tendency is heritable, but much of the divergence in our selection lines was due to epistatic effects. These results are consistent with other life history traits that are predicted to maintain more epistatic variance than additive variance and highlight the potential for epistatic variation to act as an adaptive reserve that may become visible to selection when a population is subdivided.

Genetic architecture of dispersal behaviour in the post-harvest pest and model organism Tribolium castaneum

“…Past work on Tribolium has provided evidence of a genetic basis to dispersal behaviour, which our results corroborate (Schurr and Bolduan 1967 ; Ogden 1970a , 1970b ; Ritte and Lavie 1977 ; Korona 1991 ; Ruckman and Blackmon 2020 ). We saw a rapid response to selection on dispersal, creating extreme divergence between the behaviour of high and low dispersal selection regimes over just two generations in our T. castaneum lines.…”

“…Several studies on Tribolium have demonstrated a genetic basis to dispersal through responses to artificial selection (Schurr and Bolduan 1967 ; Ogden 1970a , b ; Ritte and Lavie 1977 ; Korona 1991 ; Ruckman and Blackmon 2020 ); though many of these measured dispersal only in single-sex groups. The rapid response to selection observed across these experiments, has led some authors to postulate that the trait is controlled by very few loci (Ogden 1970a ; Ritte and Lavie 1977 ).…”

“…For example, evidence of differential dispersal in the sexes between reciprocal crosses, have led to suggestion that dispersal is controlled by a single, sex-linked locus (Ritte and Lavie 1977 ). In contrast, line cross analysis on a similar set of crosses has provided evidence that epistatic interactions across loci dominate additive effects in dispersal adaptation (Ruckman and Blackmon 2020 ). Despite considerable effort spent investigating dispersal in Tribolium little is known definitively; findings are contradictory (Ritte and Lavie 1977 ; Ruckman and Blackmon 2020 ), and many studies are only modestly replicated (Ritte and Lavie 1977 ), and/or were conducted before the availability of modern computational and molecular genetic techniques.…”

Generating and testing reagents for CRISPR/Cas9 based homologous recombination and gene drive inTribolium

“…The following strains were utilized: vermilion white (v w ), [30], GA-1, and Henderson Black (HB) [31].…”

“…Tribolium husbandry and strains: All animals were raised at 28°C on a standard flour yeast mix. The following strains were utilized: vermilion white ( v w ), [30], GA-1, and Henderson Black (HB) [31].…”