The rise of the three-spined stickleback – eco-evolutionary consequences of a mesopredator release

Abstract

Declines of large predatory fish due to overexploitation are restructuring food webs 1 across the globe. It is now becoming evident that restoring these altered food webs requires 2 addressing not only ecological processes, but evolutionary ones as well, because human-induced 3 rapid evolution may in turn affect ecological dynamics. In the central Baltic Sea, abundances of 4 the mesopredatory fish, the three-spined stickleback (Gasterosteus aculeatus), have increased 5 dramatically during the past decades. Time-series data covering 22 years show that this increase 6 coincides with a decline in the number of juvenile perch (Perca fluviatilis), the most abundant 7 predator of stickleback along the coast. We studied the interaction between evolutionary and 8 ecological effects of this mesopredator take-over, by surveying the armour plate morphology of 9 stickleback and the structure of the associated food web. First, we investigated the distribution of 10 different stickleback phenotypes depending on predator abundances and benthic production; and 11 described the stomach content of the stickleback phenotypes using metabarcoding. Second, we 12 explored differences in the relation between different trophic levels and benthic production, 13 between bays where the relative abundance of fish was dominated by stickleback or not; and 14 compared this to previous cage-experiments to support causality of detected correlations. We 15 found two distinct lateral armour plate phenotypes of stickleback, incompletely and completely 16 plated. The proportion of incompletely plated individuals increased with increasing benthic 17 production and decreasing abundances of adult perch. Stomach content analyses showed that the 18 completely plated individuals had a stronger preference for invertebrate herbivores (amphipods) 19 than the incompletely plated ones. In addition, predator dominance interacted with ecosystem 20 production to determine food web structure and the propagation of a trophic cascade: with 21 increasing production, biomass accumulated on the first (macroalgae) and third (stickleback) 22 trophic levels in stickleback-dominated bays, but on the second trophic level (invertebrate 23 The rise of the stickleback; Britas Klemens Eriksson et al. 2020 3 herbivores) in perch-dominated bays. Since armour plates are defence structures favoured by 1 natural selection in the presence of fish predators, the phenotype distribution suggest that a novel 2 low-predation regime favours sticklebacks with less armour. Our results indicate that an 3 interaction between evolutionary and ecological effects of the stickleback take-over has the 4 potential to affect food web dynamics. 5 6