Genetic and habitat complexity effects on unpredictability in escape behavior of a grasshopper species

The debate surrounding the role of genetic and environmental factors in shaping behavior has a long tradition. However, their effects on complex behaviors such as unpredictability in anti-predator strategies remain poorly understood. Behaving unpredictably when escaping predators may increase the prey's chances of survival, especially when prey can rely on a complex habitat providing camouflage and shelter opportunities. We explored the effects of genetic and environmental influences on escape strategies of the steppe grasshopper Chorthippus dorsatus. Individuals from controlled breeding had been randomly assigned to one of two environmental complexity treatments during ontogeny. We then quantified escape behavior in a large cohort through burst experiments. Using a multivariate double-hierarchical animal model, we analyzed the effects of pedigree and environmental complexity on both inter- and intra-individual variance in three components of escape behavior: flight initiation distance (FID), jump distance, and jump angle. Habitat complexity affected average jump angle, but not the average FID or jump distance, nor unpredictability in any of the three traits. Pedigree relatedness accounted for 5-6% of the total variance in average FID and average jump distance and 7% of the variance in unpredictability in jump angle. Genetic correlations suggest a behavioral syndrome structure in escape strategies that involves FID (a potential indicator of boldness). Our study demonstrates that unpredictability in escape behavior has the potential to evolve by natural selection, as some of its components are heritable. Furthermore, we show that although habitat complexity represents a strong environmental treatment, its lasting effects during ontogeny on escape behavior are minimal.

Methods
The study aimed to determine whether unpredictability in escape behavior is heritable in steppe grasshoppers (Chorthippus dorsatus) and whether habitat complexity influences developmental plasticity in unpredictability. Grasshopper offspring were obtained through a half-sib full-sib breeding design using field-caught individuals from Jena, Germany. Males (N = 51) were mated with approximately five females each (N = 249 total), ensuring a balanced color morph representation. Offspring were raised in either simple (plain white) or complex (enriched with patterned surfaces and climbing structures) habitats to assess environmental effects. Escape behavior was measured in a controlled arena where individuals were exposed to a simulated predator approach. Flight initiation distance (FID), jump distance, and jump angle were recorded using Ethovision XT software.