Fishing constrains phenotypic responses of marine fish to climate variability

Fishing and climate change are profoundly impacting marine biota through unnatural selection and exposure to potentially stressful environmental conditions. Their effects, however, are often considered in isolation, and then only at the population level, despite there being great potential for synergistic selection on the individual. We explored how fishing and climate variability interact to affect an important driver of fishery productivity and population dynamics: individual growth rate. We projected that average growth rate would increase as waters warm, a harvest-induced release from density dependence would promote adult growth, and that fishing would increase the sensitivity of somatic growth to temperature. We measured growth increments from the otoliths of 400 purple wrasse (Notolabrius funicola), a site-attached temperate marine reef fish inhabiting an ocean warming hotspot. These were used to generate nearly two decades of annually resolved growth estimates from three populations spanning a period before and after the onset of commercial fishing. We used hierarchical models to partition variation in growth within and between individuals and populations, and attribute it to intrinsic (age, individual-specific) and extrinsic (local and regional climate, fishing) drivers. At the population scale, we detected predictable additive increases in average growth rate associated with warming and a release from density dependence. A fishing-warming synergy only became apparent at the individual scale where harvest resulted in the 50% reduction of thermal growth reaction norm diversity. This phenotypic change was primarily caused by the loss of larger individuals that showed a strong positive response to temperature change after the onset of size-selective harvesting. We speculate that the dramatic loss of individual-level biocomplexity is caused by either inadvertent fisheries selectivity based on behaviour, or the disruption of social hierarchies resulting from the selective harvesting of large, dominant and resource-rich individuals. Whatever the cause, the removal of individuals that display a positive growth response to temperature could substantially reduce species' capacity to adapt to climate change at temperatures well below those previously thought stressful.