Scared to evolve? Non-consumptive effects drive rapid adaptive evolution in a natural prey population

Abstract

Predators can strongly influence prey populations through both consumptive and non-consumptive effects. Nevertheless, most studies have focused on the consumptive effects in driving evolutionary changes. By integrating experimental evolution and resurrection ecology, we tested the roles of non-consumptive and consumptive effects in driving evolution in a Daphnia magna population that experienced strong changes in fish predation pressure. All resurrected genotypes were pooled, inoculated in outdoor mesocosms, and exposed to free-fish or caged-fish treatments. Non-consumptive effects induced rapid, repeatable changes in the clonal composition and associated genotypic trait changes that were similar in magnitude and direction to those imposed by killing. Both non-consumptive and consumptive effects caused a shift towards a dominance of the high-fish period clones that can perform better under fish predation, and this may be explained by the higher intrinsic growth rate of the high-fish period clones under predation risk. The genotypic trait changes (e.g. reduced body sizes, earlier maturation, more and smaller offspring) of the Daphnia in the mesocosm experiments were in the same direction as the adaptive trait shifts observed in situ through resurrection ecology. Our results demonstrate that non-consumptive effects can induce rapid adaptive evolution and may represent an overlooked driver of eco-evolutionary dynamics.

Keywords: eco-evolutionary dynamics; experimental evolution; micro-evolution; non-consumptive effects; predator–prey interactions; resurrection ecology.

Figure 1.

Size and density of Daphnia magna at the end of the six weeks selection experiment for the three mesocosm fish predation treatments. (a) Adult size; (b) average size; (c) adult density; (d) juvenile density. Letters above the boxplots represent significantly different means based on Tukey post hoc comparisons.

Figure 2.

Clonal frequencies of Daphnia magna from the different historical fish-stocking periods in the experimental mesocosm populations at the start and at the end of the experimental evolution trial. Mean (±1 s.e.) clonal frequencies of each resurrected subpopulation are given based on five mesocosms per predator treatment.

Figure 3.

Multivariate genotypic trait values of the experimental mesocosm populations (no-fish, caged-fish and free-fish treatments) after six weeks of selection and of the three resurrected natural Daphnia magna subpopulations reflecting the population of a single pond (Oud-Heverlee Zuid) during three different historical fish-stocking periods (pre-fish, high-fish, reduced-fish periods) as reconstructed by resurrection ecology [6]. Population means are given with 1 s.e. Axes are the first two roots from a linear discriminant analysis based on 14 life-history, morphology and behaviour traits for the 18 clones used in this experiment. The traits most strongly associated with root 1 were somatic growth rate (+44.17), spine length at maturity (+38.54), size at maturity (−27.03), age at maturity (+24.35) and size of neonates (+18.64). For root 2, these were somatic growth rate (−28.65), size at maturity (+14.90), age at maturity (−19.54) and size of neonates (−12.98) (see details in electronic supplementary material, table S1). The [0,0] coordinate (intersection of hatched lines) represents the genotypic trait values for the 14 traits of the population that was inoculated in all mesocosms at the start of the selection experiment. This starting population consisted of an equal density of all 18 clones.