Artificial selection on sexual aggression: Correlated traits and possible trade‐offs

Abstract

Forced copulation is an extreme form of sexual aggression that can affect the evolution of sex‐specific anatomy, morphology, and behavior. To characterize mechanistic and evolutionary aspects of forced copulation, we artificially selected male fruit flies based on their ability to succeed in the naturally prevalent behavior of forced matings with newly eclosed (teneral) females. The low and high forced copulation lineages showed rapid divergence, with the high lineages ultimately showing twice the rates of forced copulation as the low lineages. While males from the high lineages spent more time aggressively pursuing and mounting teneral females, their behavior toward non‐teneral and heterospecific females was similar to that of males from the low lineages. Males from the low and high lineages also showed similar levels of male‐male aggression. This suggests little or no genetic correlations between sexual aggression and non‐aggressive pursuit of females, and between male aggression toward females and males. Surprisingly however, males from the high lineages had twice as high mating success than males from the low lineages when allowed to compete for consensual mating with mature females. In further experiments, we found no evidence for trade‐offs associated with high forced mating rates: males from the high lineages did not have lower longevity than males from the low lineages when housed with females, and four generations of relaxed selection did not lead to convergence in forced mating rates. Our data indicate complex interactions among forced copulation success and consensual mating behavior, which we hope to clarify in future genomic work.

The genetic basis of variation in sexual aggression: Evolution versus social plasticity

“…In each of three replicate lineages of the high FC males, we selected 48 males that forcibly copulated with the teneral females and allowed them to mate with 48 unselected, mature females from their lineage to generate the next generation. Finally, in each of three control replicate lineages, we randomly selected 48 males and allowed them to mate with 48 mature females from their lineage to generate the next generation (Dukas et al, 2020). A similar effect on FC rate, in terms of direction and magnitude, can also be generated by varying the social environment males experience prior to exposure to teneral females (Baxter & Dukas, 2017).…”

“…Evolved and plastic effects on FC. (a) Divergence in male FC rate (means ± SEMs) via artificial selection over 20 generations (based on data from: Dukas et al, 2020). Offspring of flies from generation 21 were snap frozen for RNA sequencing in this study.…”

“…There is clear variation in male tendency to force copulate that can be attributed to both genetic and environmental variation. Assays of FC rate in isogenic lines of fruit flies have shown that its broad‐sense heritability is about 0.16 (Baxter et al, 2019), and variation present in wild populations is sufficient for rapid divergence in FC rate via artificial selection (Dukas et al, 2020). FC rates have also been shown to vary in flies from the same genetic background that have been exposed to different social environments prior to exposure to teneral females.…”

“…FC rates have also been shown to vary in flies from the same genetic background that have been exposed to different social environments prior to exposure to teneral females. Males housed with no females forcibly mate at a higher rate than males who have been housed with virgin females prior to testing (Baxter & Dukas, 2017), and this effect of social experience on FC rate is of a similar magnitude to the response to artificial selection across 20 generations (Dukas et al, 2020).…”

“…In the present study, we used fruit flies as a model system for genotypic and plastic variation in sexual aggression (specifically male FC rate) to ask several questions: (1) which genes show differential expression (DE) due to evolved differences in FC rate, socially plastic differences in FC rate, or both; (2) which ontological terms are overrepresented in these sets of differentially expressed genes; (3) to what degree are gene expression changes similar (in terms of direction and magnitude) due to evolution and plasticity; and (4) do male flies with knocked down expression for candidate genes identified as important for FC variation show the expected effects on FC rate? To answer these questions, we used lineages of evolved male flies artificially selected specifically for high and low FC rate (Dukas et al, 2020), and used an established protocol to generate male flies with high and low FC rate due to prior social experience (Baxter & Dukas, 2017). We then performed whole‐transcriptome RNAseq on samples of head tissue from these males, followed by differential gene expression analysis between males with low and high FC rates.…”