Individual experience and evolutionary history of predation affect expression of heritable variation in fish personality and morphology

Abstract

Predation plays a central role in evolutionary processes, but little is known about how predators affect the expression of heritable variation, restricting our ability to predict evolutionary effects of predation. We reared families of three-spined stickleback Gasterosteus aculeatus from two populations-one with a history of fish predation (predator sympatric) and one without (predator naive)-and experimentally manipulated experience of predators during ontogeny. For a suite of ecologically relevant behavioural ('personality') and morphological traits, we then estimated two key variance components, additive genetic variance (VA) and residual variance (VR), that jointly shape narrow-sense heritability (h2=VA/(VA+VR)). Both population and treatment differentially affected VA versus VR, hence h2, but only for certain traits. The predator-naive population generally had lower VA and h2 values than the predator-sympatric population for personality behaviours, but not morphological traits. Values of VR and h2 were increased for some, but decreased for other personality traits in the predator-exposed treatment. For some personality traits, VA and h2 values were affected by treatment in the predator-naive population, but not in the predator-sympatric population, implying that the latter harboured less genetic variation for behavioural plasticity. Replication and experimental manipulation of predation regime are now needed to confirm that these population differences were related to variation in predator-induced selection. Cross-environment genetic correlations (rA) were tight for most traits, suggesting that predator-induced selection can affect the evolution of the same trait expressed in the absence of predators. The treatment effects on variance components imply that predators can affect evolution, not only by acting directly as selective agents, but also by influencing the expression of heritable variation.

Figure 1

Diagram of the experimental set-up. Arrangement of the growth tank. The tank contained a clump of artificial weed and a filter (illustrated) and was externally lined with opaque white polythene. The dashed line inside the tank indicates the position of the opaque and transparent barriers that were inserted at the onset of the live predator and chasing tests. The asterisk denotes the position where the live perch (live predator test) or perch model (chasing test) were introduced, and the arrow denotes the pattern of model chasing.

Figure 2

Sources of variation in heritabilities. For personality and morphological traits, and for each of four population–treatment groups (‘Nc’, naive population, control treatment; ‘Ne’, naive population, exposed treatment; ‘Sc’, predator-sympatric population, control treatment; ‘Se’, predator-sympatric population, exposed treatment). Stacked bars (y-axis, left) indicate the total phenotypic variance (V_P) decomposed into its additive genetic (V_A; dark grey bars) and residual (V_R; light grey bars) variance components, and dots (y-axis, right) indicate the estimated narrow-sense heritabilities (h²)±s.e. ((a) Exploration novel environment, (b) activity 2 hours after release, (c) activity 4 hours after release, (d) sociability, (e) exploration novel conspecific, (f) boldness towards predator, (g) body length, (h) body shape and (i) relative length of first dorsal spine.) We give the significance of each h² value (n.s., p>0.05; ^*p<0.05; ^**p<0.01; ^***p<0.001; for statistical analyses see table S1 in the electronic supplementary material.).