Relaxed risk of predation drives parallel evolution of stickleback behavior.

Abstract

The occurrence of similar phenotypes in multiple independent populations derived from common ancestral conditions (viz. parallel evolution) is a testimony of evolution by natural selection. Parallel evolution implies that populations share a common phenotypic response to a common selection pressure associated with habitat similarity. Examples of parallel evolution at genetic and phenotypic levels are fairly common, but the driving selective agents often remain elusive. Similarly, the role of phenotypic plasticity in facilitating early stages of parallel evolution is unclear. We investigated whether the relaxation of predation pressure associated with the colonization of freshwater ponds by nine-spined sticklebacks (Pungitius pungitius) likely explains the divergence in complex behaviors between marine and pond populations, and whether this divergence is parallel. Using laboratory-raised individuals exposed to different levels of perceived predation risk, we calculated vectors of phenotypic divergence for four behavioral traits between habitats and predation risk treatments. We found a significant correlation between the directions of evolutionary divergence and phenotypic plasticity, suggesting that divergence in behavior between habitats is aligned with the response to relaxation of predation pressure. Finally, we show alignment across multiple pairs of populations, and that relaxation of predation pressure has likely driven parallel evolution of behavior in this species.